Biotic Interactions in an Exceptionally Well Preserved Osmundaceous Fern Rhizome from the Early Jurassic of Sweden

Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Biotic interactions in an exceptionally well preserved osmundaceous fern rhizome from the Early Jurassic of Sweden

Stephen McLoughlin ⁎,BenjaminBomﬂeur

Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, S-104 05, Stockholm, Sweden article info abstract

Article history: A remarkably well permineralized osmundaceous rhizome from the Early Jurassic of southern Sweden yields Received 29 December 2015 evidence of an array of interactions with other organisms in its immediate environment. These include epiphyt- Received in revised form 29 January 2016 ism by a herbaceous heterosporous lycopsid; putative oribatid mite herbivory and detritivory (petiole and detri- Accepted 30 January 2016 tus borings and coprolites); potential pathogenic, saprotrophic or mycorrhizal interactions between fungi and Available online 6 February 2016 the host plant and its epiphytes; parasitism or saprotrophy by putative peronosporomycetes; and opportunistic

Keywords: or passive mycophagy by oribatid mites evidenced by fungal spores in coprolites. A combination of abrupt burial Osmundaceae by lahar deposits and exceedingly rapid permineralization by precipitation of calcite from hydrothermal brines Plant–animal interactions facilitated the exquisite preservation of the rhizome and its component community of epiphytes, herbivores, Fungi saprotrophs and parasites. Ancient ferns with a rhizome cloaked by a thick mantle of persistent leaf bases and Peronosporomycetes adventitious roots have a high potential for preserving macro-epiphytes and associated micro-organisms, and Mesozoic are especially promising targets for understanding the evolution of biotic interactions in forest understorey Oribatid mites ecosystems. Lycopsids © 2016 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction epiphytes. Permineralized rhizomes are particularly informative as they are commonly preserved in growth position, have anatomies that Component communities (i.e., associations of organisms trophically enable precise systematic placement, and entomb a range of exotic or- dependent on a plant host; Root, 1973) of epiphytes, arthropods and ganic remains either within their tissues or within the fibrous petiole/ fungi have been recognized in the axes and petioles of various anatom- root mantle. ically preserved fossil fern and gymnosperm taxa from the late Paleozo- A single permineralized rhizome attributed to Osmunda pulchella ic to Cenozoic (e.g., Rothwell and Scott, 1983; Rex and Galtier, 1986; (Bomfleur et al., 2015) from the Early Jurassic of Skåne, southern Tidwell and Hebbert, 1992; Genise and Hazeldine, 1995; Tidwell and Sweden, has remarkable three-dimensional preservation down to the Clifford, 1995; Weaver et al., 1997; Labandeira, 1998; Rößler, 2000; level of cell organelles and even chromosomes (Bomfleur et al., 2014). Labandeira and Phillips, 2002; Kellogg and Taylor, 2004; Lesnikowska, This fossil has proven to be useful for understanding the stasis in ploidy 1990; Osborn and Taylor, 2010; d'Rozario et al., 2011; Strullu-Derrien levels within Osmundaceae over the past 180 million years (Bomfleur et al., 2012; Slater et al., 2012, 2015; McLoughlin and Strullu-Derrien, et al., 2014), for resolving the relationships of fossil and extant represen- in press). Among these plant hosts, Osmundaceous ferns have a par- tatives of the family (Bomfleur et al., 2015), and for evaluating the ticularly rich fossil record of foliar remains, dispersed spores and timing of cladogenesis within this group of ferns (Grimm et al., 2015). permineralized rhizomes. Indeed, this family has arguably the best This unique specimen has also been the subject of popular science arti- fossil record of any group of ferns (Miller, 1967, 1971) and representa- cles that outline its significance and history of discovery (McLoughlin tives were common in the Pliensbachian of southern Scandinavia et al., 2014b; Vajda et al., 2014). The fossil fern is further investigated (Mehlqvist et al., 2009) and most of Europe (Barbacka et al., 2014). here for evidence of interactions with other organisms in its environ- Osmundaceous ferns have a thick spongy mantle of persistent leaf ment. The fossil rhizome is assessed as a case study for the broader po- bases and fine adventitious roots cloaking the central axis and this can tential of fern rhizomes to act as sources of information on the structure act as a trap for detritus from the surrounding environment, provide a of ancient leaf/root mantle micro-communities. microhabitat for invertebrates and fungi, and constitute a substrate for 2. Material and methods

⁎ Corresponding author. E-mail addresses: [email protected] (S. McLoughlin), This study is based primarily on a single permineralized rhizome, Benjamin.Bomﬂ[email protected] (B. Bomﬂeur). partially encased in volcaniclastic sedimentary rock collected in the

http://dx.doi.org/10.1016/j.palaeo.2016.01.044 0031-0182/© 2016 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). S. McLoughlin, B. Bomfleur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96 87 late 1960s or early 1970s by Korsaröd farmer Gustav Andersson and do- and genetically linked to rifting in the North Sea and opening of the nated to the palaeontological collections of the Swedish Museum of Nat- North Atlantic Ocean (Bergelin, 2009; Vajda and Wigforss-Lange, ural History, Stockholm, in November 1977. Tralau (1973) published a 2009). At least one radiometric date from central Skåne indicates short popular-science overview of the geological setting of the Korsaröd that volcanism persisted intermittently in this region until at least deposits and, later, had the fossil fern specimen cut into several blocks the mid-Cretaceous (c. 110 Ma: Bergelin, 2009). Nevertheless, palyno- from which one longitudinal and two large-format transverse thin- logical studies of the volcaniclastic deposit at Korsaröd indicate a sections were prepared (NRM S069656–S069658). The specimen is ac- Pliensbachian–early Toarcian(?) age (Bomfleur et al., 2014; Vajda companied by numerous gymnosperm wood fragments and various et al., in press). On this basis, the volcaniclastic deposits are probably rock samples from the same deposit. These were also assessed for evi- correlative with the shallow-marine Rya Formation of western Skåne dence of biotic interactions and sedimentological features indicative of a (Vajda and Wigforss-Lange, 2009). specific depositional environment. A field excavation in July 2014 at the The Pliensbachian volcaniclastic deposits at Korsaröd are mostly original collection site offered further insights into the stratigraphy of concealed beneath shallow soil cover and locally by thick Quaternary the host deposit. Thin sections were studied and photographed using an glacial moraine deposits. The volcaniclastic strata have not been Olympus BX51 transmitted light microscope and attached Olympus assigned to any formal lithostratigraphic unit, but Augustsson (2001) DP71 digital camera with Cell-D image-stacking and analytical software. proposed the informal name “Djupadal formation” for lithologically and genetically similar deposits around 17 km to the west-northwest 3. Geological setting at Djupadal (Fig. 1). The Korsaröd volcaniclastic deposit originally excavated by Gustav Andersson is located 380 m WNW of a basaltic The province of Skåne in southern Sweden hosts an extensive volcanic neck and about 10 m south of the shore of Korsaröd lake. The Triassic–Jurassic sedimentary succession that was deposited in a range volcaniclastic sediments probably represent a lahar deposit sourced of continental to shallow marine environments within several sub- from one of the nearby active volcanic centers (Vajda et al., in press). basins (Vajda and Wigforss-Lange, 2009). This succession has been The precise level at which the studied fossil fern rhizome was dated and correlated primarily on the basis of palynostratigraphy obtained from Andersson's original excavation is uncertain but there is (Guy-Ohlson, 1981; Lindström and Erlström, 2006; Vajda et al., 2013; no doubt that it was sourced from this deposit because it is partially Peterffy et al., in press), plant macrofossils (Lundblad, 1950, 1959)and encased in sediment that matches the composition of the agglomeratic marine invertebrates (Ahlberg et al., 2003). strata at the site. Re-excavation of the site in July 2014 revealed a weakly During the late Early Jurassic, sedimentation in the central part of stratified deposit exceeding 2 m thick that is dominated by greenish- Skåne was punctuated by the emplacement of numerous volcanic or reddish-weathered ash-rich lapilli tuff and agglomerate (Fig. 2A, C) necks and associated volcaniclastic deposits. The material in this study with intercalated lenses of mottled pale gray to pink clay and clayey derives from a small volcaniclastic deposit near Korsaröd, within the ash, locally with flame structures developed (Fig. 2D). The boundaries be- Central Skåne Volcanic Province (Fig. 1). This volcanic province includes tween layers are weakly defined and most beds appear to be lenticular over 100 mafic volcanic necks and several associated pyroclastic and over short distances. Fossilized wood is scattered throughout the deposit. lahar deposits—the results of strombolian volcanic activity (Eichstädt, It typically occurs as scattered angular or abraded fragments less than 1883a, 1883b; Augustsson, 2001; Bergelin, 2009). Several basanite– 10 cm long but is locally aggregated in irregular orientations (Fig. 2B). nephelinite plugs in this province have been dated at 191–178 Ma Calcite is the prevailing cement within the deposit and is the domi- based on 40Ar/39Ar whole-rock ages (Bergelin et al., 2011), and Tappe nant mineral involved in permineralization of both the fossil gymno- et al. (2016) reported a slightly younger age of 176.7 ± 0.5 Ma based sperm wood and fern rhizome. Several phases of calcite infiltration on high-precision 40Ar/39Ar dating of a nephelinite neck near Lilla occurred (Vajda et al. in press) and late-stage calcite veining transects Hagstad. This volcanism is considered to be contemporaneous with clasts and bedding fabric in some cases (Fig. 2E). Minor elemental components include Si, P, Al and Cl; traces of various metallic elements are also present at very low concentrations (Bomfleur et al., 2014). A single fi Röstånga Djupadal impression of a bennettitalean leaf fragment (Ptilophyllum sp.) in a ne Tjörnarp ash layer constituted the only foliar remains identified within the Central Skåne Volcanic Province volcaniclastic deposit (Fig. 2F).

4. The host fossil plant: O. pulchella Korsaröd 4.1. Structure and habit

SWEDEN Höör N The anatomy of O. pulchella was named and fully described by Bomfleur et al. (2015). The plant is interpreted to have grown in a pros- SKÅNE trate manner based on its rhizome having an asymmetrical distribution Västra – Skåne Ringsjön of adventitious roots (Fig. 3A D). The short creeping rhizome gave off Volcanic Helsingborg Province leaves with a basal angle of c. 25° but these may have twisted distally Östra Hörby to produce near-vertical fronds in a manner similar to extant Osmunda Ringsjön species. The rhizome, including its mantle of persistent leaf bases and adventitious roots, is only c. 37 mm in diameter suggesting that the Malmö plant was of relatively small stature (with fronds probably b50 cm tall). 5 km 10 km 5. Associated plant remains Highways Jurassic fluvial Exposures of and paralic strata volcaniclastic strata Towns 5.1. Epiphytic lycopsid roots (Höör Sandstone) Lakes Mafic volcanic plugs 5.1.1. Description fi Fig. 1. Map of Skåne, southern Sweden, showing the Korsaröd fossil locality (volcaniclastic At least two exotic roots are preserved within detritus- lled cavities deposit) within the central Skåne volcanic province. between the petiole bases of O. pulchella (Figs. 3E, 4A, B). These roots 88 S. McLoughlin, B. Bomfleur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96

2 A m B Current land surface Overburden from Gustav Andersson’s 1970s excavation 1.5 Dark brown soil with abundant roots; sparse cobbles Darkening-upward brown lapilli aggromerate

1 White–cream lenticular plastic clay Dark brown–red deeply weathered lapilli agglomerate Pale grey–pink clay (weathered ash) 0.5 Iron-stained ash with ironstone concretions and lapilli-sized clasts of black basalt

Pale grey clayey sand with mottled orange staining BOUNDARIES LEGEND 0 Sharp Gradational cl slt sand gr pb cb bd Roots Erosional C D E F

Fig. 2. A, Profile and measured section through the northern wall of the July 2014 excavation at Korsaröd. B, Block of consolidated volcanic ash containing chaotically arranged and partially charred gymnospermous wood fragments; NRM S069647. C, Ash/mud-rich lapilli agglomerate containing mostly angular mafic volcanic clasts; NRM S069643. D, Weathered, granular, lapilli tuff with flame structure arising from underlying claystone layer; NRM S069644. E, Late-stage calcite cementation and veining in a lapilli agglomerate; NRM S069646. F, Impression of a bennettitalean (Ptilophyllum sp.) leaf in volcanic ash; NRM S089751. Scale in all images represents 10 mm.

have been cut in oblique section and preserve only small amounts herbaceous lycopsids, (e.g., Fry, 1954; Leisman, 1961; Cantrill and of the central vascular system and the outermost cells of the cortex Webb, 1998; Schneider and Carlquist, 2000; McLoughlin et al., 2015a). and epidermis. The xylem tracheids are 8–24 μm wide, N210 μm long Moreover, the distribution and wedge-like insertion of root hairs in and possess pervasive pitting on all walls (Fig. 4C–E). Pits are the epidermal layer are equivalent to characters expressed in extant transversely oblong to elliptical with sporadic thin vertical or oblique lycopsids (Leavitt, 1902; Dolan, 1996). struts connecting adjacent wall thickenings (Fig. 4D). Outer cortical The roots penetrating the detritus-rich cavities between the petiole cells are thin-walled, polygonal to elliptical, 6–26 μm in minimum bases of the O. pulchella host plant are interpreted to belong to a small dimensions and 13–230 μm in maximum dimensions. A few of herbaceous epiphytic lycopsid. This plant is interpreted to have been these cells retain nuclei c. 3.5 μm in diameter (Fig. 4G) and in some living at the time of permineralization owing to the presence of pre- cases even nucleoli (Fig. 4H), almost matching the preservational served nuclear content in the outer cortical cells. quality of pith cells in the host plant (Bomﬂeur et al., 2014). Typical epidermal cells are brick-like but these are interspersed with specialized cells having a wedge-like base and a single 188-μm-long root hair 5.2. Dispersed lycopsid megaspore (Fig. 4F). 5.2.1. Description A single crushed and otherwise ill-preserved megaspore occurs 5.1.2. Remarks within a detritus-rich void between the leaf bases in the outer part of The pervasive scalariform pitting on the small number of xylem the petiole/root mantle (Figs. 3E, 5A, B). The megaspore is roughly tracheids and especially the presence of delicate cross-connecting struts 625 μm in diameter. The outer spore wall is spongy with an apparently between adjacent wall thickenings in these roots are similar to the irregular or ragged ornament. The innermost wall layer is thin and vasculature evident in the stems and roots of many ancient and modern dense. The total wall thickness is c. 35 μm. S. McLoughlin, B. Bomﬂeur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96 89

Fig. 3. Rhizome and petiole/adventitious root mantle of Osmunda pulcella. A, Transverse section of O. pulchella. B, Gray scale image of Fig. 3A, showing the asymmetrical distribution of adventitious roots (r) implying a prostrate rhizome habit. C, Longitudinal section of O. pulchella in inferred growth orientation. D, Gray scale image of Fig. 3C showing the greater concentration of adventitious roots (r) on the lower side of the rhizome. E, Gray scale image of Fig. 3C with colored areas highlighting the locations of lycopsid roots (lr), lycopsid megaspore (m), fungal hyphae (f) and putative oribatid mite coprolites (circles). Images from NRM S069656 (A, B) and NRM S069658 (C–E). Scale bars represent 10 mm (A, B) and 5 mm (C–E).

5.2.2. Remarks mid-Mesozoic based on records of dispersed megaspores (Kovach and The lack of discernible regularity in the ornament from the available Batten, 1989) and macrofossils (Pigg, 2001; McLoughlin et al., 2014a). cross-section precludes identiﬁcation to any taxon used for dispersed It is likely that the preserved megaspore was produced by the same epi- megaspores. Herbaceous lycopsids were widely distributed in the phytic lycopsid that produced the roots described above. 90 S. McLoughlin, B. Bomﬂeur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96

Fig. 4. Epiphytic lycopsid root associated with the petiole-adventitious root mantle of Osmunda pulchella. A, Lycopsid root with preserved vascular tissue and outermost cortex/epidermis; arrows indicate root hairs. B, Slightly crushed lycopsid root within a dense mass of organic debris between O. pulchella petioles. C, Scalariform elliptical pitting on the xylem tracheids of an epiphytic lycopsid root. D, Details of lycopsid root tracheid pitting; arrows indicate slender oblique to vertical struts across some pores. E, Enlargement of lycopsid root tracheid pitting. F, Wedge-shaped base (top) of a root hair (passing downward) of a lycopsid root. G, Cellular contents preserved in the outermost cortex of an epiphytic lycopsid root. H, Enlargement of a lycopsid root cell nucleus with an indistinct central nucleolus. All images from NRM S069658. Scale bars represent 250 μm (A, B), 50 μm (C), 25 μm(F),10μm (D, E, G) and 5 μm (H). S. McLoughlin, B. Bomﬂeur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96 91

5.3. Dispersed sporangial fragments Excavation margins are characterized by sharply truncated cells. Exca- vations occur both outside the vascular crescent and within the area 5.3.1. Description enclosed by the inner sclerenchymatous crescent (Fig. 6A–C). Several Sporangial fragments in the form of chains of robust annulus cells areas between the petiole bases are relatively sparse in organic detritus are preserved dispersed within the organic matrix between the petiole and may also represent zones of excavation. Several of these excava- bases of O. pulchella (Fig. 5C, D). The crescentic annuli reach 225 μm tions, both within and between the petioles of O. pulchella, contain long, with the largest cells up to 36 μmwideand50μm in radial diam- spherical–ellipsoidal pellets (38–220 μm in maximum diameter) that eter. Cell walls are up to 3.5 μm thick; the outer wall of each cell is slight- are composed of angular cell wall fragments and opaque bodies. In ly inflated. some cases, pellets of two discrete size ranges are evident within an excavation (Fig. 6C). At least one pellet contains a dark spherical body, 5.3.2. Remarks which is 10 μm in diameter (Fig. 6F). The pellets have an irregular to These remains are more robust than typical osmundaceous fern spo- slightly diffuse surface (Fig. 6E–H). rangial annuli, which generally are weakly developed (Hewitson, 1962; Phipps et al., 1998). These remains are possibly dispersed spo- 6.1.2. Remarks rangial fragments from a more derived leptosporangiate fern growing The excavations were probably produced by oribatid mites based in the immediate environment of the host plant. A diverse array on their size, shape and surface texture (Labandeira et al., 1997), al- of leptosporangiate ferns (especially representatives of Cyatheaceae, though no exoskeleton components have yet been identified. These Dicksoniaceae, Matoniaceae/Dipteridaceae and Pteridaceae) are pellets are very similar to putative oribatid mite coprolites recorded known from dispersed miospores in the surrounding sediments from a broad range of late Paleozoic and early Mesozoic gymnosperm (Bomfleur et al., 2014; Vajda et al. in press). woods (e.g., Crepet, 1972; Weaver et al., 1997; Kellogg and Taylor, 2004; Seyfullah et al., 2009; Feng et al., 2010, 2015; Osborn and 5.4. Dispersed miospore Taylor, 2010; Feng, 2012; Tidwell et al., 2013), lycopsid stems (Labandeira et al., 1997), fern rhizomes (Tidwell and Clifford, 1995; 5.4.1. Description Rößler, 2000; d'Rozario et al., 2011) and permineralized peats (Hilton A single laevigate, triangular, trilete microspore is preserved in detri- et al., 2001; Strullu-Derrien et al., 2012; Slater et al., 2012, 2015). In tus close to the lycopsid megaspore described above (Fig. 5E). The spore post-Triassic ecosystems, coleopterans, and subsequently isopterans, is ill-preserved, somewhat distorted, c. 28 μm in diameter, with a gaping became increasingly important as borers of wood and other tissues aperture. (Labandeira et al., 1997; Grimaldi and Engel, 2005). However, there is no evidence in terms of regularity of the boring traces or coprolite 5.4.2. Remarks shape to favor attribution of the damage in O. pulchella to either of Several laevigate miospores potentially matching this poorly pre- those groups. served specimen have been reported from the surrounding sediments The presence of nuclei in some of the parenchyma cells of the [e.g., Cyathidites minor Couper, 1953; Deltoidospora toralis (Leschik) O. pulchella petiole cortex, in which these cavities and coprolites are pre- Lund, 1977; Cibotiumspora jurienensis (Balme) Filatoff, 1975](Bomfleur served suggests that the consumer was herbivorous in the strict sense et al., 2014; Vajda et al., in press). Such spores are potentially attributable rather than detritivorous, although there is no evidence of wound re- to various leptosporangiate fern groups: Matoniaceae, Dicksoniaceae, sponses to the damaged areas. By contrast, coprolites in the detritus- Cyatheaceae or Dipteridaceae (Balme, 1995). filled cavities between the petioles may reflect strict detritivory by the putative mite producers. Similar damage is evident in the stem cortex 5.5. Plant detritus and petiole bases of the tree fern Itopsidema vancleavei (Daugherty, 1960) from the Late Triassic of Arizona (Ash, 2000). The presence of 5.5.1. Remarks coprolites of two discrete size ranges within some excavations suggests Fine (generally b160 μm diameter) irregular plant fragments are the activities of more than one animal or, more likely, persistence of the preserved extensively in voids between the roots and leaf bases of consumer in the same excavation over an extended period of growth O. pulchella. In some cases, the debris has accumulated on one side of through more than one instar (Feng et al., 2010). the inter-petiole cavity providing a geopetal structure (Fig. 5C). The The smooth, dark, spherical body preserved in one coprolite may organic fragments appear to be a mixture of cell wall, cuticle and represent a fungal spore. Its solitary presence, and the absence of globular–spicular opaque humic gels or other decay products. Much of associated hyphae that would indicate saprotrophy of the fecal pellet, the debris may represent fragments of non-consumed tissue resulting suggests that its occurrence is the result of passive or opportunistic (fac- from oribatid mite excavations or subaerially entrapped debris shed ultative) rather than targeted (obligate) mycophagy. McLoughlin and from the surrounding vegetation. Some of the fine debris may derive Strullu-Derrien (in press, fig. 7c) illustrated a similar solitary fungal from disaggregation of mite coprolites. body within an oribatid mite coprolite interpreted to represent passive Fine globular and spicular opaque precipitates are common in other or opportunistic ingestion. This contrasts with the apparent targeted permineralized woods and peats (Taylor et al., 2015; McLoughlin and mycophagy of some Permian oribatid mites, whereby the coprolites Strullu-Derrien, in press) and are commonly attributed to solidified are composed almost exclusively of fungal remains (Slater et al., 2012, resins or consolidated humic gels, especially where pale contraction pl. 6.3, 6.4). rims are evident. However, Klymiuk et al. (2013) notedthatatleast some similar opaque bodies within plant tissues can represent biomi- 7. Fungal interactions metic mineral (e.g., pyrite) precipitates. 7.1. Hyphae 6. Arthropod interactions 7.1.1. Description 6.1. Excavations and coprolites Only a few sparse thread-like structures in the root/petiole mantle of O. pulchella are potentially attributable to fungal hyphae. Delicate 6.1.1. Description (1.5 μm wide), branching, but otherwise apparently featureless, Excavations up to 715 μm in diameter are evident within the soft thread-like structures occur within some petiole parenchyma cells of parenchymatous tissues of the inner part of some O. pulchella petioles. the host plant (Fig. 5H). A few of these threads appear to penetrate 92 S. McLoughlin, B. Bomfleur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96 S. McLoughlin, B. Bomfleur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96 93 through the walls of adjacent cells. More distinct, apparently aseptate, 8. Discussion and conclusions hyphae (c. 4 μm wide) are evident passing along the center of a root hair and penetrating the cortical tissues of an epiphytic lycopsid rootlet From just a small portion of an O. pulchella permineralized rhizome (Fig. 5F). and its sheath of petioles and adventitious roots (Fig. 7A, B) it is possible to discern a complex array of biotic interactions in the immediate growth environment of this Early Jurassic fern (Fig. 7C–H). These inter- 7.1.2. Remarks actions include: Identification of the more delicate branching threads is equivocal. They potentially represent ill-preserved pathogenic or saprotrophic fungal hyphae invading necrotic tissues of the host plant. However 1. Epiphytism (by a herbaceous heterosporous lycopsid on the rhizome Klymiuk et al. (2013) noted that some mineral precipitates within of O. pulchella)(Fig. 7C) plant tissues can take on a filamentous form reminiscent of hyphae. 2. Invertebrate herbivory (borings in O. pulchella petioles) and The tubular filament penetrating the lycopsid root hair (Fig. 5F) is a detritivory (feeding on the detritus between petiole bases) probably more convincing fungal hypha. Root hairs may have facilitated the by oribatid mites (Fig. 7D) hypha's access to the interior of the lycopsid root as they do in many 3. Entrapment of organic detritus from the surrounding vegetation in modern plants (Imhof et al., 2013). Because the cortical cells of the the spongy root/petiole rhizome mantle, which may have provided root are poorly preserved, we could not identify whether arbuscles additional nutrients for the host plant and its epiphytes (Fig. 7E) were developed in the cortex, which might indicate whether the fungus' 4. Possible fungal interactions (pathogenic or saprotrophic) with interaction with the plant was mycorrhizal (cf. Uphof, 1920; Martinez O. pulchella in the form of putative hyphal invasion of parenchyma- et al., 2012; Muthukumar and Prabha, 2013). On the other hand, neither tous tissues of the petiole bases (Fig. 7F) did we find evidence of appositions or other modifications in the root 5. Lycopsid epiphyte–fungal interactions (mycorrhizal or pathogenic) hairs or cortical cells that might indicate a response to the invasion of in the form of hyphae penetrating the root cortex via root hairs a pathogen (cf. Lucas, 1998; Leroux et al., 2011). (Fig. 7I) 6. Putative peronosporomycete (parasitic or saprotrophic) invasion of 7.2. Fungal or fungi-like reproductive structures O. pulchella petiole parenchyma and inter-petiole detritus (Fig. 7G) 7. Facultative mycophagy by oribatid mites evidenced by fungal spores 7.2.1. Description in coprolites (Fig. 7H) Three types of putative fungal spores or fungi-like reproductive Although no foliage of O. pulchella is preserved, surveys of fossil structures occur in the studied sample. Type 1 is represented by ellipsoi- floras elsewhere indicate that Jurassic Osmundaceae leaves were regu- dal spores 13–20 μm in minimum dimensions, 16–29 μminmaximum larly attacked by arthropod folivores (McLoughlin et al., 2015b). dimensions, and ornamented by weak ridges or a reticulum (Fig. 5G). Osmundaceous ferns probably hosted a complex community of perma- These occur close to the epidermis of one of the lycopsid roots that nent and itinerant small arthropods, fungi and plant epiphytes in the has been invaded by a fungal hypha. Type 2 constitutes globose bodies, understorey of the Swedish Early Jurassic forests. Beyond this, the host c. 16 μm in diameter with prominent knob-like (bullate) ornamenta- sediments contain a wealth of dispersed pollen, spores, wood and tion. These bodies occur either in the detritus between the petiole charcoal that indicate a complex forest community subject to episodic bases (Fig. 5I) or within the parenchymatous petiolar tissues (Fig. 5J) fires and other forms of disturbance in an active volcanic land- of O. pulchella. One of these has a truncate base that may represent a hy- scape under a moderately seasonal climate (Vajda et al., in press). phal attachment. Type 3 is represented by laevigate, thick-walled, sphe- Osmundaceous ferns were a prominent understorey element in this roidal bodies, 15–34 μm in diameter with a prominent slit-like aperture vegetation and were probably involved in various competitive inter- (Fig. 5K, L) These bodies occur scattered through the detritus between actions with neighboring plant species. If the identification of the oogonia the petiole bases. of peronosporomycetes is correct, then this implies regularly moist conditions for the growth of O. pulchella and this is consistent with the gen- 7.2.2. Remarks eral habitat preferences of extant Osmunda and associated herbaceous We were unable to identify any close morphological matches lycopsids (Wagner and Smith, 1993). We envisage that the studied between the poorly preserved spores of type 1 and fossil or modern O. pulchella rhizome was part of a fern- and conifer-rich vegetation occu- spores. Although many late Paleozoic and early Mesozoic water pying a topographic depression in the landscape (moist gully) that was mould reproductive bodies have more elaborately branched ap- engulfed by one or more lahar deposits in the Pliensbachian. pendages (Strullu-Derrien et al., 2011; Krings et al., 2011; Slater Fibrous root/petiole mantles around osmundaceous rhizomes et al., 2013), the shape, sparsely bullate ornament, and truncate in general represent ideal preservational settings for a host of epi- base of type 2 bodies are reminiscent of the characters of some fossil phytes, micro-herbivores, parasites, saprotrophs and otherwise (Mississippian) peronosporomycete oogonia from France (Taylor accidentally entrapped fine organic remains. Several earlier reports et al., 2015, fig. 13.43) and some extant Phytophthora oogonia of fossil osmundaceous rhizomes have documented the presence of (Yang et al., 2013). Type 3 spores have few characters to facilitate invertebrate coprolites (e.g., Schopf, 1978; Tidwell and Clifford, identification. Numerous laevigate fungal spores have longitudinal 1995) and fungal remains (Kidston and Gwynne-Vaughan, 1907; clefts (e.g., Coniochaeta ascospores of vanGeeletal.,2011); but Gould, 1970). Other ferns with a similar thick mantle of fibrous some algal zygospores/aplanospores can also have a similar mor- roots and persistent leaf bases or multiple axes (e.g., Psaronius, phology (van Geel, 2001). zygopterid ferns and Tempskya) have an equivalent potential as

Fig. 5. Plant, animal, fungi and fungi-like interactions with Osmunda pulchella. A, Lycopsid megaspore and coprolites entrapped between petioles of O. pulchella. B, Enlargement of lycopsid megaspore with a dense inner wall layer and spongy outer layer. C, Plant debris accumulation on one side of a cavity between adventitious roots and petioles of O. pulchella.D.Enlargement of fern sporangial annulus from Fig. 5C. E, Trilete spore preserved adjacent to the megaspore in Fig. 5B. F, Fungal hypha penetrating the root hair of an epiphytic lycopsid. G, Type 1 fungi- like spores preserved adjacent to the base of an epiphytic lycopsid root hair. H, Putative fungal hyphae within and penetrating between the cortical cells of an O. pulchella petiole. I, Type 2 fungus-like body (possible peronosporomycete oogonium) among detritus between O. pulchella petiole bases. J, Type 2 fungus-like body (possible peronosporomycete oogonium) within the parenchymatous cells of an O. pulchella petiole. K, L, Thick-walled type 3 fungi-like spores with slit-like apertures preserved among detritus between O. pulchella petioles. Images from NRM S069658 (A, B, E–L) and NRM S069656 (C, D). Scale bars represent 500 μm(A,C),100μm(2B),50μm (D), 25 μm (F, G) and 10 μm (E, H–L). 94 S. McLoughlin, B. Bomﬂeur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96

Fig. 6. Possible oribatid mite interactions with Osmunda pulchella. A, Transverse section of petiole showing two excavated areas filled with coprolites. B, Enlargement from Fig. 6A: coprolite-filled excavation in the inner cortex outside the vascular crescent. C, Enlargement from Fig. 6A: coprolite-filled excavation within the area enclosed by the inner sclerenchymatous crescent; arrow indicates a patch of diminutive coprolites possibly derived from an early stage of the borer's development. D–H, Enlargements of individual coprolites showing details of shape, surface texture and content. Note isolated fungal spore in Fig. 6F (arrowed). Images from NRM S069657 (A–C, F) and NRM S069658 (D, E, G, H). Scale bars represent 500 μm(A),250μm(C),100μm(B),50μm(D)and25μm(5E–H). S. McLoughlin, B. Bomfleur / Palaeogeography, Palaeoclimatology, Palaeoecology 464 (2016) 86–96 95

to have facilitated the remarkable preservation of this rhizome and its component community of epiphytes, herbivores/detritivores, and putative saprotrophs, symbionts and parasites.

Acknowledgments

Financial support by the Swedish Research Council (VR grants 2014- 5234 to S.M. and 2014-5232 to B.B.) is gratefully acknowledged. Vivi Vajda (NRM) is thanked for organizing the excavation at the Korsaröd fossil site in July 2014, funded by the Swedish Research Council (VR), Lund University Carbon Cycle Centre (LUCCI), and the Royal Swedish Academy of Sciences. Excavation at the site was assisted by students from the Department of Geology, University of Lund. The members of Tjörnarps Sockengille (Tjörnarp) are thanked for access to the fossil locality. We thank Dr. R. Rößler and an anonymous reviewer for their con- structive comments on the manuscript.

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