Review of Palaeobotany and Palynology 235 (2016) 120–128

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Review of Palaeobotany and Palynology

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Plant-arthropod and plant- interactions in late Permian gymnospermous woods from the Bogda Mountains, Xinjiang, northwestern China

Mingli Wan a,b,c, Wan Yang c,d,LujunLiua,b,JunWanga,b,⁎ a Department of Palaeobotany and Palynology, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China b State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China c Geology and Geophysics Program, Missouri University of Science and Technology, Rolla, MO 65409, USA d Key Laboratory of Petroleum Resources Research, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China article info abstract

Article history: Several lines of evidence of plant-arthropod and plant-fungus interactions are documented from the Received 9 April 2016 Wuchiapingian Wutonggou low-order cycle (approximate equivalent to the Wutonggou Formation) in Tarlong Received in revised form 30 August 2016 valley, southern Bogda Mountains, Xinjiang Uygur Autonomous Region, northwestern China. Fossil wood, Accepted 10 October 2016 Septomedullopitys szei Wan, Yang et Wang, contains differentially-damaged areas. Spindle-shaped pockets in Available online 11 October 2016 the fossil wood occurring in the secondary xylem are commonly free of organic remains. They are comparable Keywords: in appearance to modern white-pocket rot caused by fungi. The tracheid walls around the decomposed areas Plant-arthropod interaction are degraded from the middle lamellae to outer layers. Abundant branching and septate fungal hyphae in the Plant-fungus interaction decayed areas, ray parenchyma and tracheid lumina indicate that fungi are responsible for the wood decay. Septomedullopitys szei These fungi are partially regarded as basidiomycetes because of the occurrence of clamp connections. According Angara Flora to the characteristic damages they caused to the host, ascomycetes are also viable candidates of the fungi because Wuchiapingian large parts of hyphae are without certain clamp connections. The other damaged excavations are branched and Paleoecology maze-like borings and galleries, which are filled with abundant fungal hyphae, cellular debris and spheroidal to ovoidal, dark-colored coprolites, ranging from 26 to 128 μm in diameter. The size, shape, and surface texture of these coprolites indicates that the coprolites are the feces of ancient oribatid mites. The fungal hyphae, coprolites, and degraded excavations in the pith of the late Permian wood suggest that wood-rotting and -boring were not limited to the xylem. © 2016 Elsevier B.V. All rights reserved.

1. Introduction the Permian (Labandeira et al., 1997; Labandeira, 1998a, 1998b; Kellogg and Taylor, 2004; Feng, 2012; Feng et al., 2010, 2012, 2015; D'Rozario Land plants and arthropods are two major macroscopic sources for et al., 2011; Slater et al., 2012; Falcon-Lang et al., 2015). However, only biodiversity on the planet, and have historically provided the basic evo- few arthropod detritivores within gymnospermous woods have been re- lutionary history and ecological structure to continental ecosystems ported from the middle-latitude areas in the same time period. (Labandeira, 2006a). Plant-arthropod interactions are crucial to the evo- Similarly, fungi have had a long and complex geological history and lution of terrestrial ecosystems (Labandeira, 1998a, 2006b, 2006a, played an important role in modern ecosystems (Taylor and Taylor, 2006b). Once plants became established on the land, a number of plant- 1997; Taylor et al., 2009, 2014). Fungi are the major decomposers of arthropod interactions evolved rapidly, having involved all the early higher plants in both modern (Otjen and Blanchette, 1982, 1984, plants (Labandeira, 2006b; Labandeira, 2007). Arthropod detritivores in 1985; Dighton et al., 2005) and ancient (Stubblefield and Taylor, 1986, Paleozoic terrestrial ecosystems have been recorded in both high-latitude 1988) ecosystems. The interactions between fungi and plants in terres- and tropical terrestrial ecosystems from the late Silurian to the end of trial ecosystems have been well documented during the late Paleozoic (Dennis, 1970; Tiffney and Barghoorn, 1974; Pirozynski, 1976; Wagner and Taylor, 1981, 1982; Stubblefield and Taylor, 1986, 1988; ⁎ Corresponding author at: Department of Palaeobotany and Palynology, Nanjing Stubblefield et al., 1984, 1985a, 1985b; Hass et al., 1994; Taylor and Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China. Taylor, 1997, 2000; Krings et al., 2007, 2010, 2011, 2012). However, E-mail address: [email protected] (J. Wang). the reported plant-fungus interactions have been observed mainly

http://dx.doi.org/10.1016/j.revpalbo.2016.10.003 0034-6667/© 2016 Elsevier B.V. All rights reserved. M. Wan et al. / Review of Palaeobotany and Palynology 235 (2016) 120–128 121 from materials of Euramerica and Gondwana Floras, providing little in- Şengör and Nat'lin, 1996; Ziegler et al., 1997; Scotese, 2001; Yang et formation on the Angara Flora. al., 2010). The uppermost Carboniferous to Lower Triassic sedimentary There are several investigations of plant-arthropod interactions in rocks in the half graben include conglomerate, sandstone, shale, and the Paleozoic of China. Studies of plant-arthropod interactions in the Pa- minor limestone and volcanic rocks deposited in fluvial, and lacustrine leozoic of China (Glasspool et al., 2003; Wang et al., 2009; Feng et al., environments (Fig. 1,D;Yang et al., 2007, 2010). The permineralized 2010, 2012; D'Rozario et al., 2011; Feng, 2012) are purely based on ma- stems of Septomedullopitys szei examined in current study were collect- terials from the Cathaysia Flora. China is the only country where the four ed from a sandstone unit at the base of Wutonggou low-order cycle at major floras: Cathaysia, Angara, Euramerica and Gondwana, were de- the southwestern Tarlong Section (Wan et al., 2014; Fig. 1,D).Thesand- veloped during the Carboniferous and Permian (Shen, 1995). No fossil stone unit is on the top of a coarsening-upward shale-sandstone succes- evidence of plant-arthropod interactions in the other three floras of sion and has a concave erosional base. It was interpreted as a China was reported. In addition, the records of fungus-plant association distributary channel fill on a deltaplain above the delta-front deposit are rare in the Paleozoic of China (Wang, 1997). (Yang et al., 2010). The age of the fossil-bearing interval is probably In this study, we present evidence of the co-occurrence of fungal hy- early Wuchiapingian, as determined from cyclostratigraphic correlation phae and arthropod coprolites are present in the late Permian gymno- of the southwestern Tarlong Section with the northeastern Tarlong Sec- sperm wood Septomedullopitys szei Wan, Yang et Wang from southern tion where three U-Pb zircon radiometric ages of the low-order cycle Bogda Mountains in Xinjiang Uygur Autonomous Region, which is a part are available (Yang et al., 2010). The stems are parallel to the bedding of the Angaran phytoprovince in the Permian (Fig. 1,A,B;Meyen, 1981, plane, suggesting that they were transported from upstream or nearby 1982, 1997; Sun, 1989). Extensive features of fungal decay and feeding be- interdistributary area and deposited in a distributary channel on the havior of oribatid mites are observed in the xylem tracheids and pith. Two delta plain (Wan et al., 2014). distinctive types of damage to the wood are documented and attributed The fossil wood genus Septomedullopitys Lepekhina has been found to the activities of wood-rotting fungi and oribatid mites. Results of this only in the upper Permian of Angaran phytoprovince (Lepekhina and study provide additional information about the co-occurrence of plant-ar- Yatsenko-Khmelevsky, 1966; Lepekhina, 1972). It is characterized by thropod and plant-fungus interactions in the late Permian. the combination of secretory ducts within the septate pith, endarch pri- mary xylem and Protophyllocladoxylon-type secondary xylem. S. szei 2. Geological setting, materials, and methods consists of reticulate pith with straight secretory ducts and several par- enchymatous bands that are distinct from the Kuznetsk (Wan et The research area is located in the Tarlong-Taodonggou half graben, al., 2014). The characteristics of S. szei could be easily distinguished from southern foothills of the Bogda Mountains, bordering the northwestern other relative Palaeozoic pycnoxylic groups, including pteridosperms, margin of the Turpan Basin, Xinjiang Uygur Autonomous Region, north- and ginkgophytes. Cordaitaleans from Cathaysia and Euramerica Floras western China (Fig. 1,A,B;Yang et al., 2007, 2010). The half graben was possess septate pith and endarch primary xylem which resemble S. szei located at the easternmost Kazakhstan Plate in the Permian. (Fig. 1,C; (Wang et al., 2003; Hilton et al., 2009a,b; Taylor et al., 2009). However,

Fig. 1. Geographic and geologic maps of the research area. A) and B) Maps showing the location of the fossil stem of Septomedullopitys szei Wan, Yang et Wang. I - Angara province in the Junggar-Hinggan Region; II - Cathaysia-Euramerica-Angara mixed province; III - Cathaysia province; IV - Gondwana province; V - Angara province in Tarim Plate (Shen, 1995). The collection site is shown by the wood stem symbol in (B), which is in the Permian Angaran phytoprovince (Meyen, 1981, 1982, 1997; Sun, 1989). The collection site as shown by the wood stem symbol in (B) is ~12 km north of the town of Daheyan in the southern foothills of the Bogda Mountains, northwestern China. C) Paleogeographic map during late Permian showing the fossil site (star) in the easternmost Kazakhstan Plate at the mid-latitude NE Pangea. Modified after Scotese (2001). D) Geological map of the Tarlong-Taodonggou area showing the fossil collection site (wood stem symbol) in southwestern Tarlong. After Yang et al. (2010). 122 M. Wan et al. / Review of Palaeobotany and Palynology 235 (2016) 120–128 they are different from S. szei in the lack of secretory ducts throughout D800 digital single-lens reflex camera. Images were taken equipped the whole pith. Reticulate pith in S, szei is distinguishable from the with a Leica DM5000 compound microscope and Leica DC 500 digital pith in Cordaitaleans. Therefore, S. szei is tentatively attributed to a pos- microscope camera system. The specimens and the slides are stored in sible coniferous affinity. the Paleobotanical Collection of the Nanjing Institute of Geology and A thin-section microscopic study of the stems indicates that they are Palaeontology, Chinese Academy of Sciences, with a registration well silicified. Large specimens were photographed by using a Nikon number PB21686.

Fig. 2. Characteristic morphological features of decay areas in the stem of Septomedullopitys szei Wan, Yang et Wang. A) Photomicrograph of a transverse section showing numerous excavations (white cavities) around the axis in the pith and in the xylem. The cavities in the pith show a circular and elongate morphology. Those in the xylem have various morphologies and are radially distributed. The black arrow points to a tunnel similar to a crack, with a large number of spheroidal and ovoidal, dark-colored coprolites. The white patches are cavities filled with calcite. B) Photomicrograph of a transverse section of the xylem, showing the various morphologies of the decayed areas (white cavities) and irregular distribution. The cavities are mostly elongated, some elliptical and circular. C) Photomicrograph of a transverse section of the xylem, showing that the white calcite-filled cavities of decay areas are confined within two adjacent growth interruptions or cut across the growth interruptions. D) Photomicrograph of a radial section of the xylem, showing the morphology of the decayed areas containing spindle- to circular-shaped pockets filled with white calcite. E) Photomicrograph of a transverse section of the stem, showing pith in the lower part and xylem with radiating rays in the upper part. Many spheroidal and ovoidal, dark-colored coprolites (black arrows) are preserved in the peripheral areas of the pith. F) Photomicrograph of a radial section of the stem, showing an area of intense wood decay. Abundant coprolites are present in the straight tunnel (white arrow) and network systems (black arrows) of the xylem. G) Photomicrograph of a radial section of the stem, showing extensively degraded xylem filled with densely spheroidal and ovoidal, dark-colored coprolites. H) Photomicrograph of a radial section of the stem, showing the degradation of the pith. Abundant coprolites are present in the straight tunnel (white arrow). M. Wan et al. / Review of Palaeobotany and Palynology 235 (2016) 120–128 123

3. Observations C, D). The second type occurs as branched and/or maze-shaped borings and galleries, filled with abundant fungal hyphae, cellular debris, sphe- 3.1. Wood damaged patterns roidal to ovoidal, dark-colored coprolites (Fig. 2, E, F, G). In addition, the pith is damaged (Fig. 2, H). However, the damaged areas in the pith vary Areas showing tissue damaged occur throughout the stems of in morphology and commonly contain numerous fungal hyphae, cellu- Septomedullopitys szei (Fig. 2, A, B). Two types of geometry of decayed lar debris and coprolites (Fig. 3, A, B, C, D). The borings and coprolites are areas were observed in the xylem. The first type occurs as spindle- distributed surrounded to the anomalous parenchymatous bands in the shaped pockets which are commonly free of organic remaining (Fig. 2, pith (Fig. 3,C).

Fig. 3. Decayed excavations containing coprolites within the pith and xylem of Septomedullopitys szei Wan, Yang et Wang stem. A) Photomicrograph of a radial section of the pith, showing a decayed cavity of the pith containing brown spherical coprolites (black arrow). The white patches are cavities filled with calcite. B) Photomicrograph of a transverse section of the pith, showing decay cavities in the pith containing spheroidal and ovoidal, dark-colored coprolites (black arrows). White arrows demonstrate the secretory ducts with opaque contents. C) Photomicrograph of a transverse section of the pith, showing borings and coprolites distributed surrounded to the anomalous parenchymatous bands (black arrow). PB = parenchymatous band. D) Photomicrograph of a transverse section of the pith, showing spheroidal and ovoidal, dark-colored coprolites present in the peripheral part of the pith. E) Photomicrograph of a radial section of the xylem, showing the boring within the secondary xylem, filled with moderately distributed coprolites. F) Photomicrograph of a radial section of the xylem, showing a complex network system containing abundant fungal hyphae, coprolites, and cellular debris. Spheroidal and ovoidal, dark-colored coprolites are loosely distributed. G) Photomicrograph of a radial section of the xylem, showing the moderately distributed spheroidal and ovoidal, dark-colored coprolites near ray parenchymatous cells. H) Photomicrograph of a radial section of the xylem, showing the loosely distributed spheroidal and ovoidal, dark-colored coprolites. 124 M. Wan et al. / Review of Palaeobotany and Palynology 235 (2016) 120–128

The dimension and shape of the first type of damaged areas vary entirely between the adjacent growth interruptions (Fig. 2,C,black greatly. Individual decay cavities are circular to elliptical in transverse arrows) or alternatively cutting across the growth interruptions section and up to 1.8 mm wide (Fig. 2, B, C); and are spindle-shaped (Fig. 2,C,whitearrows). in longitudinal section, up to 2.9 mm long (Fig. 2, D). These cavities In the second type of decay areas, some of the borings are intercon- are commonly free of cellular debris but may contain some cell wall re- nected with each other to form a complex maze-shaped system as large mains. Some fungal hyphae, coprolites and cracked plant remains occur galleries in longitudinal sections (Fig. 3, E, F, G). Such borings are also in a few cavities. Partially decayed tracheids are common along the mar- transversally distributed within the woods. Most of the borings and gal- gins of the cavities. Decay cavities occur throughout the secondary leries are filled with packed coprolites and plant remains, as well as xylem (Fig. 2, B). In addition, the cavities exhibit either distribution some fungal hyphae (Fig. 3,F,G).

Fig. 4. The decay pattern of xylem and fungal hyphae within the decayed areas of Septomedullopitys szei Wan, Yang et Wang. A) Photomicrograph of a transverse section of the xylem, showing degraded tracheids, of which the compound middle lamellae are completely removed (black arrows). Both the compound middle lamellae and other wall layers are all degraded with only a veneer of S3 layers left (white arrow). B) Photomicrograph of a transverse section of the xylem, showing that the compound middle lamellae and other wall layers of tracheids are all degraded with only faint S3 layers left (black arrow). C) Photomicrograph of a radial section of the pith, showing a curved, branched and septate extending through the parenchymatous cells (black arrow). D) Photomicrograph of a radial section of the pith, showing excavations containing spheroidal and ovoidal, dark-colored coprolites and a branched fugal hypha (black arrow). E) Photomicrograph of a transverse section of the xylem, showing branched and septate hypha extend through the tracheids (black arrow). F) Photomicrograph of a radial section of the xylem, showing the branched and septate (black arrow) hypha. G) Photomicrograph of a radial section of the xylem, showing branched and septate hypha within a decayed cavity. H) Photomicrograph of a radial section of the xylem, showing a hypha with . M. Wan et al. / Review of Palaeobotany and Palynology 235 (2016) 120–128 125

Many tracheids are extensively degraded. Commonly the compound removed. Consequently, the adjacent tracheids are separated with middle lamellae of these tracheids are completely removed (Fig. 4,A). each other from the compound middle lamellae. In the second pattern, The radial and tangential walls are separated from the neighboring cell the compound middle lamellae, primary wall and partially the second- walls. In some cases, both the compound middle lamellae and tracheid ary wall of tracheids are removed, only some S3 layer left, reflecting a wall layers are degraded with only blurred S3 layers left (Fig. 4,A,B). cellular shape. Finally, all of the organic contents of the tracheidal walls are decomposed. Progressing degradation formed the damaged 3.2. Coprolites pockets within the wood. This process caused progressive thinning and ultimate destruction of the compound middle lamellae and primary Coprolites are found in both pith and xylem. Spheroidal and ovoidal cell walls, and finally, the secondary cell walls. To date the best evidence coprolites in the pith occur not only in the pith chambers (Fig. 3,A,B,C, for fossil wood decay process comes from Permian silicified D), but also in the parenchymatous cells (Fig. 3, B, C). In transverse sec- permineralizations collected from Antarctica (Stubblefield and Taylor, tions, the coprolites are present in the peripheral and central parts of 1986). The underground axis Vertebraria was degraded by basidiomy- decayed areas in the pith (Figs. 2,E;3,D). cetes with two decay patterns. The first pattern includes spindle-shaped The borings and galleries within the xylem are commonly filled with pockets and removed middle lamellae, and is very similar to that in our coprolites (Fig. 2,F, G). These coprolites have a similar shape to those in fossil wood. The second pattern involves cell wall degradation in the pith. They are either densely packed (Fig. 2, G) or loosely piled (Fig. Vertebraria, including removal in the direction of middle lamellae and 3, F, G, H). In some cases, the coprolites occur together with decayed tra- corners of the cells being the last to be degraded. In contrast, the cheids and fungal hyphae. The diameter of the coprolites ranges from 26 decay process in our fossil wood occurs in an opposite direction, from to 128 μm(Fig. 3, H). Coprolites from the pith and xylem are all com- the middle lamellae to the secondary cell walls. posed of unidentifiable plant fragments. There are three types of fungal wood rot: brown, white and soft (Otjen and Blanchette, 1986; Schmidt, 2006). Each type can be related to a par- 3.3. Fungal remains ticular group of organisms with characteristic enzymatic activities that develop unique patterns of decay and distinctive macroscopic and micro- Fungal hyphae are abundant in the xylem and pith. Branched and scopic modifications of wood structure (Stubblefield and Taylor, 1986). septate hyphae are also present in the pith with a similar form to White rot refers to the degradation of cellulose, hemicelluloses, and lignin those within the xylem tracheids. They either extend through the par- by fungi (Schmidt, 2006). White rot fungi are responsible for most lignin enchymatous cells or scatter over the degraded areas (Fig. 4,C,D,E, degradation (Otjen and Blanchette, 1984; Geib et al., 2008), among many F), ranging from 1.2 to 9.8 μm in diameter. In the xylem, they are gener- microorganisms that can cause wood decay. White rot can be subdivided ally oriented parallel to the long axis of the tracheids (Fig. 4, G). In some macroscopically into white-pocket, white-mottled, and white-stringy instances, individual hypha can be traced over a vertical distance of rots (Blanchette, 1984; Schmidt, 2006), and microscopically into simulta- about 0.8 mm as they extended through the wood. Branches of hyphae neous and successive rots (Liese, 1970). White-pocket rot can be distin- are commonly thinner than the parent hyphae (Fig. 4, F, G). The septa of guished from other types of white rots in several aspects (Blanchette, hyphae are spaced irregularly, connected to the hyphal walls at right an- 1980; Otjen and Blanchette, 1984). It is characterized by discrete elongat- gles, and commonly associated with slight constrictions of the hyphae ed or spindle-shaped pockets of decayed wood separated by sound wood, (Fig. 4, F). Hyphae are commonly present in a relatively straight or and by white cellulose tissues without lignin. A unique characteristic of slightly curving form (Fig. 4, F, G). Septate branching and septate hy- white-pocket rot is a diffusible lignin-degrading enzyme system. Micro- phae always occur in the decayed pockets and partially degraded tra- scopically, white-pocket rot is characterized by the removal of the middle cheids (Fig. 4, F, G). Hyphae in the xylem exhibit not only simple but lamellae resulting in separation of cells (Blanchette, 1980; Otjen and also clamp connection (Fig. 4, H). The clamp connection is simple and Blanchette, 1984, 1985; Schmidt, 2006). Both the macro- and microscopic relatively large. Branching occurs occasionally by hyphal proliferation features of degradation in Septomedullopitys szei including spindle- through clamp connection (Fig. 4,H). shaped pockets, apparently delignified areas, and the patterns occurred on the tracheid walls are consistent with those of the white-pocket rot. 4. Discussion Thus,itisproposedthatwhite-pocketrotbyfungihadformedthespin- dle-shaped decay in the stem of S. szei. The xylems of the permineralized trunks of Septomedullopitys szei The fungi found in Septomedullopitys szei are well preserved. Their contain anatomically well and poorly-preserved areas. The poorly-pre- major characteristic features, branching and septation with clamp con- served areas contain abundant cavities. The origin of these cavities is nection are similar to the extant basidiomycetes. White-pocket rot is complex because they are commonly filled with coprolites, cellular de- commonly caused by members of and rarely of Ascomyco- bris, fungal hyphae and sediments. Possible causes of a perforated fossil ta in modern terrestrial ecosystem (Schmidt, 2006). Modern basidiomy- wood include wood boring arthropods, differential mineralization and cetes play an important role in the carbon cycle by decaying organic fungal activities (Stubblefield and Taylor, 1986). Differential mineraliza- matter, including wood, a process that returns available nutrient back to tion is excluded because such pseudoborings in a generally silicified the ecosystem (Otjen and Blanchette, 1986; Dighton et al., 2005; Taylor wood are actually isolated groups of calcified cells (e.g. Fisk and Fritz, et al., 2009, 2014). White rot basidiomycetes are the only fungi capable 1984). The retained organic matters and visible cellular outlines in the of degrading all cell wall components, including lignin, hemicelluloses perforated areas of our stems, and selectively-removed compound mid- and cellulose (Otjen and Blanchette, 1986). The fungi that caused the cav- dle lamellae of the cell walls are distinct from the pseudoborings caused ities decay and cell wall degradation in the xylem of S. szei are probably by differential mineralization. Fungal activity and attack by wood boring basidiomycetes due to the occurrence of the clamp connections, which arthropods are indicated by the occurrence of fungal hyphae and copro- is a positive characteristic of basidiomycetes (Krings et al., 2011). Howev- lites in our stems, and by the macroscopic and microscopic decay pat- er, ascomycetes remain to be a viable candidate because not all of the hy- terns similar to those in modern plants attacked by fungi and phae described here is with clamp connections. On the basis of no arthropods (e.g. Blanchette, 1980, 1984; Otjen and Blanchette, 1985, reproductive structure connected with them being preserved, it is im- 1986; Schmidt, 2006). probable to know the hyphae concerned here at a lower taxonomic level. Three geometric patterns of cellular wall degradation are present at The interactions between fungi and plants reflecting a new appreci- the margins of pockets in the damaged xylem of Septomedullopitys szei. ation of fossil fungi as integral parts of ancient ecosystems have been the In the first pattern, the heavily-lignified middle lamellae between adja- focus of modern paleomyclological studies (Stubblefield and Taylor, cent tracheids and the primary tracheidal walls are completely 1988). Mutualism, saprophytism and have been reported in 126 M. Wan et al. / Review of Palaeobotany and Palynology 235 (2016) 120–128 fossil plants from the Paleozoic and Mesozoic (e.g. Stubblefield et al., Ponomarenko (2010) described a kind of possible trace by beetles 1985a; Krings et al., 2007; Harper et al., 2012). Nevertheless, in most from the middle Permian in a coniferous wood from the Kama River cases the relationship between a fossil fungus and its host is difficult Basin. A system of tunnels and shafts are preserved in their fossil to determine because the only available information is the morphology wood, and 2.8 mm in diameter. Their length ranges from about 5 to of a single phase of the life cycle of the fungus (Stubblefield et al., 1984; 73 mm. The tunnels and shafts were speculated as the feeding trace of Taylor and Krings, 2005). The interactions of fungi with vascular plants Permocupedidae or Tshekardocoleidae, which is different from the bor- are usually measured in the fossil record based on microscopic re- ings produced by oribatid mites in our fossil wood. Other Paleozoic re- sponses that fungal invasion, including axial parenchyma, various cords of arthropod-plant interaction from the Angara Flora include types of resinous deposits, abnormal growth rings, thickened secondary feeding traces on the pinnules of peltaspermous plants (Vasilenko, walls (appositions) (Stubblefield and Taylor, 1986; Taylor and Krings, 2007, 2011; Krassilov and Karasev, 2008; Aristov et al., 2013). The oc- 2005; Krings et al., 2007; Harper et al., 2012). In present material, the re- currence of oribatid mite trace fossils in our wood extends the paleogeo- sponse is absent probably because the bulk of cells in the gymnosperm graphical distribution of these causative wood-boring arthropods. wood at mature are largely dead, which is not readily respond to fungal Paleozoic wood-borings by oribatid mites are mainly recorded in attacks, or because the host tree had been died when the fungi penetrat- coal balls and silicified peats, which were deposited in wetland environ- ed. The present material shows diffusedly and evenly decayed areas all ments (Cichan and Taylor, 1982; Labandeira et al., 1997; Labandeira, over the wood rather than the precisely defined pockets of rot. Accord- 1998a, 1998b; D'Rozario et al., 2011; Slater et al., 2012). Some mite- ing to Creber and Ash (1990), the damaged wood attacked by sapro- bored woods were deposited in riparian habitats (Feng et al., 2010; phytic white-pocket rot fungi would present similar distribution and Césari et al., 2012). According to their sedimentological and paleobotan- dimension of decayed areas. Therefore, although it is difficult to abso- ical data, the host trees were living in a fairly humid environment but lutely evaluate the interactions between fungi and Septomedullopitys with short water stress. Based on evidence from Paleozoic and Mesozoic szei, the fungi occurred in current fossil wood are more likely to be borings and coprolites from the Antarctica, Kellogg and Taylor (2004) saprophytic. concluded that insects are more prolific wood borers in dry environ- The coprolites inside the borings, galleries, and branched tunnels in ments and oribatid mites are dominant in moist environments, because Septomedullopitys szei suggest a typical arthropod-plant interaction fair- the Mesozoic records of insect wood borings mostly occur in the fossil ly common in fossil and modern ecosystems. It is difficult to know the woods grew in drier environments (Walker, 1938; Linck, 1949; arthropods concerned here at a lower taxonomic level because most Tidwell and Ash, 1990). The common Gleysols and Argillisols, and of the Paleozoic arthropod fauna has been replaced by modern lineages some Histosols capping meandering stream and deltaic deposits in the after the end-Permian mass extinction (Labandeira and Sepkoski, 1993; Wutonggou low-order cycle suggest that the early Wuchiapingian cli- Selden, 1993; Labandeira, 1994); and direct evidence, such as body fos- mate of Tarlong where Septomedullopitys szei grew was humid to sub- sils, is lacking in Middle Devonian to Early Jurassic records (Labandeira humid with weak precipitation seasonality (Yang et al., 2010; Thomas et al., 1997). All of the coprolites range from 32 to 116 μm in diameter, et al., 2011). The absence of true growth rings and the presence of irreg- and are within the size range of those produced by oribatid mites. Mod- ular growth interruptions in our fossil wood indicate that the host trees ern collembolans produce coprolites of a comparable size to the oriba- were living under a humid climate but with short-lived, irregular tids, but with a rough, irregular surface, which is different from droughts (Wan et al., 2014). This ecological environment is also the fa- smooth, oval coprolites of oribatid mites (Labandeira et al., 1997). Ac- vored habitat of modern oribatid mites, which generally like living con- cording to the size, shape, surface texture, contents, and form of the sur- ditions with elevated humidity (Badejo et al., 2002; Lindberg et al., rounding tissues of coprolites proposed by Labandeira et al. (1997),the 2002; Noti et al., 2003; Taylor and Wolters, 2005; Tsiafouli et al., 2005; borings, galleries, tunnels, and coprolites in this study were probably Lindberg and Bengtsson, 2006; Gergócs and Hufnagel, 2009). produced by oribatid mites. Oribatid mites primarily decompose the plant tissues by directly or The coprolites in the excavations of both xylem and pith in indirectly interacting with the decomposing microbiota, especially sap- Septomedullopitys szei share the same morphology and dimension, and rophytic fungi (Clement and Haq, 1984; Norton, 1985; Afifi et al., 1989; fairly-well to loosely compacted. Regarding their dimension and mor- Renker et al., 2005), and as a result, comminute the plant materials to be phology, the coprolites in the pith may also indicate the activity of an- integrated into the soil (Labandeira et al., 1997). A number of species of cient oribatid mites. Modern oribatid mites consume both hard plant modern mites ingest fungal material or mixtures of wood and fungal tissues, such as wood and bark, and softer parenchymatous tissues material (Martin, 1979). Laboratory experiments indicate that oribatid and reduce them into particulate debris (Labandeira et al., 1997). Sever- mites mainly live on saprophytic fungi rather than litter material al findings showed that some groups of ancient oribatid mites fed pref- (Luxton, 1966; Martin, 1979). Most modern oribatid mites in decaying erentially on harder, lignified tissues of secondary xylem and whereas wood are probably fungivores rather than strict xylophages (Norton, other groups selectively fed on much softer parenchymatous tissues 1985; Seastedt et al., 1989). Tripartite fungus-plant-arthropod interac- (Labandeira et al., 1997; Kellogg and Taylor, 2004; Feng et al., 2010, tions are frequent in modern terrestrial ecosystem (Hatcher, 1996; 2012, 2015). Different feeding behaviors and strategies may indicate Harirington, 2005; Stout et al., 2006), and have been recorded from fos- the presence of different species, although they produce very similar sil evidence (Banks and Colthart, 1993; Barthel et al., 2010; D'Rozario et coprolites (Feng et al., 2010). Therefore, the coprolites contained in al., 2011; García Massini et al., 2012). Plant-arthropod and plant-fungus the pith and the xylem of S. szei may probably represent different spe- interactions have co-occurred in Septomedullopitys szei,assuggestedby cies of oribatid mites. the common preservation of both coprolites and fungal hyphae in the Evidence for arthropod detritivores in the Paleozoic is found in re- borings and tunnels of the pith and xylem of the fossil wood. However, cords as early as Late Silurian (Labandeira, 1998b, 2006a, 2006b, the coprolites and fungal hyphae are never conjoined with each other in 2007) and till up to the latest Permian (Feng, 2012; Feng et al., 2010; our wood. Fungal remains and are not observed within the cop- D'Rozario et al., 2011), but is temporally and geographically patchy rolites, which are composed of unidentified plant fragments. Therefore, (Strullu-Derrien et al., 2012). Arthropod detritivores in the Paleozoic it is difficult to determine the degree of association between the fungi are well documented in the low-latitude Euramerican (Baxendale, and producers of the coprolites in our fossil wood. 1979; Cichan and Taylor, 1982; Labandeira et al., 1997; Feng et al., 2015) and Cathaysian (Feng et al., 2010, 2012; D'Rozario et al., 2011; Acknowledgements Feng, 2012), and high-latitude Gondwanan floras (Weaver et al., 1997; Kellogg and Taylor, 2004; Césari et al., 2012; Slater et al., 2012), We thank Dr. Jonathon Obrist and Zhixin Li of Missouri University of but are rarely found in mid-latitude Angara Flora. Naugolnykh and Science and Technology, and Mr. Shengwu Mei of Nanjing Institute of M. Wan et al. / Review of Palaeobotany and Palynology 235 (2016) 120–128 127

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