Alcheringa: An Australasian Journal of Palaeontology

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The architecture of Permian glossopterid ovuliferous reproductive organs

Stephen Mcloughlin & Rose Prevec

To cite this article: Stephen Mcloughlin & Rose Prevec (2019) The architecture of Permian glossopterid ovuliferous reproductive organs, Alcheringa: An Australasian Journal of Palaeontology, 43:4, 480-510, DOI: 10.1080/03115518.2019.1659852 To link to this article: https://doi.org/10.1080/03115518.2019.1659852

Published online: 01 Oct 2019.

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=talc20 The architecture of Permian glossopterid ovuliferous reproductive organs

STEPHEN MCLOUGHLIN and ROSE PREVEC

MCLOUGHLIN,S.&PREVEC, R. 20 September 2019. The architecture of Permian glossopterid ovuliferous reproductive organs. Alcheringa 43, 480–510. ISSN 0311-5518

A historical account of research on glossopterid ovuliferous reproductive structures reveals starkly contrasting interpretations of their architecture and homologies from the earliest investigations. The diversity of interpretations has led to the establishment of a multitude of genera for these fossil organs, many of the taxa being synonymous. We identify a need for taxonomic revision of these genera to clearly demarcate taxa before they can be used effectively as palaeobiogeographic or biostratigraphic indices. Our assessment of fructification features based on extensive studies of adpression and permineralized fossils reveals that many of the character states for glossopterids used in previous phylogenetic analyses are erroneous. We interpret glossopterid fertiligers to have been borne in loose strobili in which individual polysperms represent fertile cladodes of diverse morphologies subtended by a vegetative leaf or bract. Polysperms within the group are variously branched or condensed with ovule placement ranging from marginal to abaxial, in some cases occurring on recurved branchlets or in cupule-like structures. Glossopterid polysperms of all types are fringed by one or two ranks of wing-like structures that may represent the remnants of megasporophylls that were, ancestrally, developed on the fertile axillary shoot. Glossopterid fertiligers have similarities to the condensed bract/ovuliferous scale complexes of conifer cones, but comparisons with Mesozoic seed-ferns are hindered by insufficient data on the arrangement and homologies of the ovule- bearing organs of the latter group. Nevertheless, glossopterid polysperms differ from the ovuliferous organs of Mesozoic seed-ferns by longitudinal versus transverse folding, respectively. Stephen McLoughlin [[email protected]], Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden; Rose Prevec [[email protected]], Department of Earth Sciences, Albany Museum, 40 Somerset Street, Makhanda, 6139, Eastern Cape, South Africa, and Department of Botany, Rhodes University, PO Box 94, Makhanda, 6140, Eastern Cape, South Africa. Received 8.4.2019; revised 21.8.2019; accepted 21.8.2019.

Key words: Glossopteris, fructifications, reproductive biology, Gondwana, plant anatomy, phylogeny.

SINCE Glossopteris was named by Brongniart in the (Surange & Chandra 1975, Crane 1985, Doweld 2001), early 1800s, this group of extinct seed plants has cordaitaleans or gnetaleans (Schopf 1976), conifers aroused widespread debate regarding its architecture, (Rigby 1978, Anderson & Anderson 1985)or systematics and phylogenetic relationships. Sergei angiosperms (Plumstead 1956a, Retallack & Dilcher Meyen (1987, p. 159) wrote of glossopterids ‘Probably 1981, Melville 1983b). Other workers (e.g., Pant 1977, no other group of fossil plants can be named where the Taylor et al. 2009) have recognized that glossopterids morphology, systematics and phylogeny were subject to possess a suite of characters that are either not shared such tremendous errors and controversy as the by other plant groups (autapomorphic characters) or Arberiales’ (¼Glossopteridales or Dictyopteridiales). that are shared ancestrally by many plant groups Understanding the architecture and structural homolo- (highly plesiomorphic characters) and, as such, are gies of glossopterid reproductive organs has proven phylogenetically uninformative. Consequently, glossop- particularly challenging. An anonymous reviewer for a terids are commonly placed in a unique family (Sporne manuscript submitted to the American Journal of 1965), order (Srivastava & Srivastava 2016), class ‘ Botany went so far as to state The glossopterid repro- (Banerjee 1984, Anderson et al. 2007) or phylum (Le ductive structures are in my own humble opinion the Roux & Anderson 1977) without necessarily any paleobotanical equivalent of a root canal, and I am implied close relationship to other plant groups. ’ thankful that others are so happy to take care of them . Since the earliest description of a glossopterid Over the course of nearly 200 years, various work- ovuliferous fructification (Dictyopteridium Feistmantel, ers have argued that glossopterids are affiliated with 1881), over 40 genera have been established to accommo- – the ferns (Brongniart 1828 38, Feistmantel 1880, 1890, date the morphologically diverse range of reproductive Arber 1905), cycads (Lacey et al. 1975, Leary 1993), organs attached to, or associated with, glossopterid foliage ginkgoopsids (Meyen 1987), Mesozoic seed-ferns (Fig. 1A–N). Unfortunately, many of these genera are ß 2019 Geological Society of Australia Inc., Australasian Palaeontologists clearly synonyms established on the basis of misinterpre- https://doi.org/10.1080/03115518.2019.1659852 tations of fructification architecture resulting from

Published online 01 Oct 2019 ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 481

Fig. 1. Selection of glossopterid ovuliferous reproductive organs preserved in various modes and representative of the four families: Dictyopteridiaceae (A–H), Rigbyaceae (I, J), Arberiaceae (K, L), and Lidgettoniaceae (M, N). A, Dictyopteridium sporiferum Feistmantel, 1881 482 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Fig. 1 (Continued) (lectotype), mould of fertile surface showing numerous diminutive seed scars; Raniganj or Barakar formations (probably Lopingian), Gopal Prasad, Talchir Coalfield, India; GSI5210. B, Scutum leslii Plumstead, 1952 emend. Prevec, 2011, mould of fertile surface bearing around 25 seed scars on the receptacle surrounded by a broad fluted wing; Vryheid Formation (Cisuralian), Vereeniging, Karoo Basin, South Africa; BP/2/ 13735. C, Ottokaria bengalensis (holotype), polysperm with dentate wing and long pedicel attached to the petiole of a Glossopteris communis Feistmantel, 1876 leaf; Karharbari Formation (Cisuralian), Giridih Coalfield, India; GSI7287. D, Senotheca keiraensis McLoughlin, 2012b, slender polysperm attached to the midrib of a Glossopteris leaf; Illawarra Coal Measures (Lopingian), Grahams Mine, Mt Keira, southern Sydney Basin, Australia; MMF2913. E, Karingbalia inglisensis (McLoughlin, 1990a) McLoughlin 2016 (paratype), mould of fertile surface of polysperm showing distally swept wing; Black Alley Shale (Lopingian); tributary of Stony Creek, 48 km west-southwest of Rolleston, Bowen Basin, Australia; UQF76126a. F, Gladiopomum acadarense (Anderson & Anderson, 1985) Adendorff, McLoughlin & Bamford, 2002, mould of non-ovuliferous surface of a polysperm with broad wings and a well-defined apical extension; ?Vryheid Formation (Cisuralian), Cedara, northeastern Karoo Basin, South Africa; BP/2/16329a. G, Bifariala intermittens (Plumstead, 1958a) Prevec in Prevec et al., 2008, mould of fertile surface of polysperm showing striate secondary wing in apical region overlying smooth primary wing, which is exposed in lateral and basal areas; Vryheid Formation (Cisuralian), quarries, 6 km south of Vereeniging, Karoo Basin, South Africa; VM/03/3205/63. H, Elatra leslii (Thomas, 1921) Prevec, 2014, polysperm with distally extended secondary wing, and hooded, primary wing partially concealed by mould of seed-bearing surface of receptacle; Vryheid Formation (Cisuralian), quarries, 6 km south of Vereeniging, Karoo Basin, South Africa; BP/2/7433. I, Nogoa biloba (McLoughlin, 1990a) McLoughlin, 2012c (holotype), mould of fertile surface of fan-shaped polysperm bearing two large seed scars; Burngrove Formation (Lopingian), Minnie Creek, Bowen Basin, Australia; UQF76211. J, Rigbya arberioides, Lacey, van Dijk & Gordon- Gray, 1975, fan-shaped receptacle borne on a long, slender pedicel; Normandien Formation (Lopingian), Mooi River, northeastern Karoo Basin, South Africa; NM/1650. K, Arberia leeukuilensis Anderson & Anderson, 1985, planated polysperm with seed attachments on recurved marginal appendages; Vryheid Formation (Cisuralian), Leeukuil Quarries, Vereeniging, Karoo Basin, South Africa; BP/2/14284. L, Arberia hlobanensis Anderson & Anderson, 1985, variably branched polysperm with terminal seed scars rimmed by scale-like flanges; Vryheid Formation (Cisuralian), Hlobane Colliery, northern Karoo Basin, South Africa; BP/2/15893. M, ‘Partha’ (¼Lidgettonia) belmontensis White, 1978, slender scale-like leaf bearing four cupular polysperms on short pedicels; Newcastle Coal Measures (Lopingian), Belmont, northern Sydney Basin, Australia; AMF46525. N, Lidgettonia mooiriverensis Anderson & Anderson, 1985, four stellate cupular polysperms attached in opposite pairs by moderate-length pedicels to either side of the midline of a scale-like glossopterid leaf; Normandien Formation (Lopingian), Mooi River, northeastern Karoo Basin, South Africa; NM/1596a. different styles of preservation. Various authors have Material and methods attempted to organize the genera of glossopterid repro- This study is the result of many years of collective — ductive organs into families and orders the numerous research on glossopterid reproductive organs from sites resulting classification schemes differing as a conse- spanning the entirety of Gondwana. Analyses were car- quence of contrasting emphases placed on, for example, ried out using mainly incident light microscopy of the shape of the fructifications, the number of reproduct- impressions and compressions and transmitted light ive units attached to a subtending leaf, the morphology of microscopy of cellulose acetate peels and thin-sections the associated leaf, or the number of seeds per fructifica- of three-dimensionally preserved (permineralized) tion (Surange & Chandra 1975, Banerjee 1984, Anderson specimens. Additional details of key morphological & Anderson 1985, Maheshwari 1990,Doweld2001). characters have been acquired via scanning electron Although four families are usually recognized within microscopy. The studied material has been collected glossopterids (Dictyopteridiaceae, Lidgettoniaceae, during our own fieldwork and by many previous Rigbyaceae, Arberiaceae: Anderson & Anderson 1985), researchers, and is now stored in numerous museum no taxonomic scheme has been universally accepted collections. The principle studied collections are housed because the architectures of the fructifications, even at a in the: Evolutionary Studies Institute (formerly the very basic level (e.g., radial versus bilateral symmetry), Bernard Price Institute: BP) of the University of the remain disputed. Alternative models of the basic structure Witwatersrand, Johannesburg; Vaal Teknorama of the ovuliferous fructifications (polysperms) of glossop- Museum (formerly the Vereeniging Museum: VM), terids have resulted in their interpretation variously as fer- Veereniging; KwaZulu-Natal Museum (NM), tile axillary shoots, solitary megasporophylls attached to Pietermaritzburg; Albany Museum, Makhanda axillary shoots, megasporophylls fused to a subtending (Grahamstown); Queensland Museum (QM), University leaf, or fertile pinnae forming part of an otherwise normal of Queensland (UQ) and Geological Survey of leaf (Surange & Chandra 1975, Schopf 1976, Retallack Queensland (GSQ), Brisbane; Australian Museum & Dilcher 1981, Meyen 1984, Anderson & Anderson (AM), Sydney; Geological Survey of New South Wales 1985,Kato1990, McLoughlin 1990c, 2011b,Taylor& (MM), Londonderry, New South Wales; Geoscience Taylor 1992, Doyle 2006). Australia (GA), Canberra; Museum Victoria (MV), Here we review the history of research on glossop- Melbourne; University of New England (UNE), terid ovuliferous fructification architecture. We re-evalu- Armidale; Geological Survey of India (GSI), Calcutta; ate the structural interpretations of the reproductive Botany Department of the University of Calcutta organs and their subtending leaves, and provide a revised (UCB), Calcutta; Birbal Sahni Institute of architectural model that should facilitate construction of Palaeosciences (BSIP), Lucknow; Museo Argentino de a more consistent generic and suprageneric taxonomy, Ciencias Naturales ‘Bernardino Rivadavia’ (BA Pb), and provide a more meaningful basis for phylogenetic Buenos Aires; La Plata Museum (LP Pb), La Plata; analyses incorporating glossopterids as a whole. Department of Paleontology and Stratigraphy (DPE) of ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 483

Fig. 2. Schematic diagram showing the terminology used to describe morphological features of glossopterid ovuliferous reproductive organs. A, Example of an Arberiaceae polysperm with ovuliferous appendages (branches) inserted marginally and over one (abaxial) surface of a flattened branch system. B, Example of a Rigbyaceae polysperm with dichotomous ovuliferous branches partially fused at the base to form a flattened fan-shaped lamina. C, Example of a Lidgettoniaceae fertiliger with an adnate axillary branch system giving rise to multiple cupule-like polysperms (inset); dashed line delimits zone of apical thickening. D–F, Examples of scutiform Dictyopteridiaceae polysperms with variable development of a marginal wing and seed scars restricted to one surface of the receptacle. the Federal University of Rio Grande do Sul (UFRGS), University of Queensland. Illustrations were produced Porto Alegre; University of Kansas (KU), Lawrence; using Adobe Creative Cloud software. The Natural History Museum (NHMV), London; and the Swedish Museum of Natural History (NRM), Stockholm. Photographs were taken using Canon 40D Morphological terminology or Sony Cybershot digital cameras, or a Sony Soundvision digital camera attached to a Zeiss Stemi Various terms have been used previously to denote the SV6 dissecting microscope with low angle illumination whole or parts of glossopterid ovuliferous organs. of the specimen from the upper left. Scanning electron Schopf (1976), Meyen (1984, 1987) and Anderson & micrographs were obtained using a Philips 505 SEM at Anderson (1985) adopted the terms ʻ polyspermʼ and the Centre for Microscopy and Microanalysis, the ‘fertiligerʼ for the ovule-bearing organ and the 484 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Fig. 3 (Continued) compressed polysperm embedded in the rock matrix. C, Features highlighted of the mould of the polysperm when split through the plane of the primary wing. D, Features highlighted of the mould of the polysperm when split through the plane of the secondary wing. Prior position of shed seeds indicated with dashed lines. Modified with permission from Prevec et al., (2008).

fructification-leaf complex, respectively. Although these terms have not gained broad usage in more recent studies of glossopterids or other plant groups, we retain them in their original sense (Fig. 2A–F), since they have merit over alternatives, such as ‘cone’, ‘megasporophyll’ or ‘gonophyll’, in that they do not imply structural homologies with the reproductive organs of other plant groups. The term ‘receptacle’ is used for the central ovule-bearing body of capitulum- or shield-like (here designated ‘scutiform’—a term favoured over the more unwieldy alternative ‘dictyopteridioid’), cupulate, or flabellate fructifications (Fig. 2D–F). The term ‘wing’ refers to any thin transversely striate flange, either entire or dissected, projecting from the periphery of the receptacle (Fig. 2C–F). In some cases (e.g., Bifariala and Elatra), glos- sopterid fructifications bear two marginal wings. These are designated ‘primary’ and ‘secondary’ wings accord- ing to the scheme established by Prevec et al. (2008) and Prevec (2014)(Figs 3, 4). Fructifications are almost exclusively planated dorsiventrally, with seeds borne on only one surface; the reverse side revealing only venation patterns (Fig. 2C, F). The only exception to this rule occurs in some species of Arberia, in which some ovules may be borne marginally. We refer to the alternate sides of these dorsiventral organs as simply the ‘seed-bearing surface’ and the ‘veined surface’. The raised cushions or depressions (depending on original morphology and preservational style) on the seed- bearing surface of the receptacle in scutiform and cupu- late forms, and at branch termini in flabellate or branched forms, are identified as seed scars (Figs 5, 6). The central protuberance or depression typically seen in the centre of each scar is designated a ‘tubercle’ or ‘pit’, respectively. The stalks inserted at the base of the receptacle in scutiform and cupulate fructifications, and the primary stalk of flabellate or branched forms, are designated the ‘pedicel’.

Architecture of glossopterid ovuliferous organs Central issues related to polysperm morphology Some of the uncertainty related to phylogenetic place- ment of glossopterids has arisen from fundamentally different interpretations of the morphology of the ovu- Fig. 3. Double-winged morphology evident in Bifariala intermittens liferous fructifications. This applies especially to the (Plumstead, 1958) emend Prevec in Prevec et al., 2008. A, Reconstruction of a polysperm showing the ovuliferous surface and scutiform (dictyopteridioid) fructifications and the fol- two wings highlighted by different colours. B, Cross-section of a lowing discussion focusses primarily on that group. ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 485

Fig. 4. Double-winged morphology evident in Elatra leslii (Thomas, 1921) Prevec, 2014. A, Reconstruction of the polysperm showing the ovuliferous surface, two wings highlighted by different colours, and showing planes of hypothetical cross-sections. B, Reconstructed transverse sections of the polysperm showing different expressions of the hooded primary wing at various positions. C, Features highlighted of the mould of the polysperm when split through the plane of the secondary wing. D, Reconstruction of polysperm showing the plane of a hypothetical longitudinal section. E, Modelled longitudinal section of the compressed polysperm showing the recurved (hooded) nature of the primary wing. F, Modelled longitudinal section of the mould of the polysperm with key features highlighted. S ¼ seed. Modified with permission from Prevec et al. (2008). 486 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Fig. 5. Details of the variation in seed-scar morphology on the receptacles of various glossopterid fructifications. A, Dictyopteridium sporiferum Feistmantel, 1881; Kamthi Formation (Changhsingian), Mahanadi Basin, India; BSIP35031. B, Ottokaria transvaalensis Plumstead, 1956b emend Anderson & Anderson, 1985; Vryheid Formation (Cisuralian), northern Karoo Basin, South Africa; BP/2/13606. C, Scutum leslii Plumstead, 1952 emend. Prevec, 2011; Vryheid Formation (Cisuralian), Vereeniging, Karoo Basin, South Africa; BP/2/13735. D, Plumsteadia semnes Rigby, 1978; Blair Athol Coal Measures (Artinskian), Blair Athol Basin, Australia; GSQF5505. E, Plumsteadia sp.; Mersey Coal Measures (Sakmarian–Artinskian), Tasmania Basin, Australia; AMF66563a. F, Gonophylloides waltonii (Plumstead, 1958)Maheshwari,1965;Vryheid Formation (Cisuralian), Vereeniging, Karoo Basin, South Africa; BP/2/14239a. G, Plumsteadia jensenii McLoughlin, 1990b;IllawarraCoal Measures (Lopingian), northern Sydney Basin, Australia; AMF120071. H, Karingbalia inglisensis (McLoughlin, 1990a) McLoughlin, 2016; Black Alley Shale (Wuchiapingian), western Bowen Basin, Australia; UQF76119a. I, Senotheca keiraensis McLoughlin, 2012b; Illawarra Coal Measures (Lopingian), southern Sydney Basin, Australia; MMF2913. J, Scutum sp. cf. S. leslii Plumstead, 1952 of Tewari et al.(2012); Barakar Formation ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 487

Fig. 5 (Continued) (?Kungurian–?Guadalupian), Wardha Basin (Godavari Superbasin), India; BSIP39682. K, Estcourtia vandijkii Anderson & Anderson, 1985; Normandien Formation (Lopingian), eastern Karoo Basin, South Africa; NM/1276a. L, Bifariala intermittens (Plumstead, 1958a) Prevec in Prevec et al., 2008; Vryheid Formation (Cisuralian), northern Karoo Basin, South Africa; BP/2/13963. M, Cupule of ‘Partha’ raniganjensis Surange & Chandra, 1973c; Kamthi Formation (Changhsingian), Mahanadi Basin, India; BSIP36617. N, Cupule of Lidgettonia lidgettonioides (Lacey et al., 1975) Anderson & Anderson, 1985; Normandien Formation (Lopingian), eastern Karoo Basin, South Africa; NM/1576b. O, Cupules of Denkania indica Surange & Chandra 1973b; Raniganj Formation (Lopingian), Mahanadi Basin, India; BSIP35034. P, Rigbya arberioides Lacey, van Dijk & Gordon-Gray, 1975; Normandien Formation (Lopingian), northeastern Karoo Basin, South Africa; NM/1644a. Q, Nogoa biloba (McLoughlin, 1990a) McLoughlin, 2012c; Burngrove Formation (Lopingian), central Bowen Basin, Australia; UQF76211. R, Arberia brasiliensis Lundqvist, 1919; Rio Bonito Formation (Artinskian), southern Parana Basin, Brazil; NRMS048024-02. S, Arberia hlobanensis Anderson & Anderson, 1985; Vryheid Formation (Cisuralian), northern Karoo Basin, South Africa; BP/2/15893. Scale bars ¼ 1mm for A–C, E–K, M–Q; 5 mm for D, L, R, S.

Fig. 6. Scanning electron micrographs of seed attachment points on Karingbalia inglisensis (McLoughlin, 1990a) McLoughlin, 2016; Black Alley Shale (Wuchiapingian), western Bowen Basin, Australia; UQF79474. A, Mould of fertile surface showing the shape and distribution of seed scars. B, Individual seed-scar mould showing seed insertion point (tubercle ¼ T) set in a depression on the receptacle. C, Inverted and rotated image of B providing a replica of the seed scar on the original fructification, showing seed insertion point (pit ¼ P) set on a raised platform on the receptacle. D, Seed scar in plan view showing prominent files of epidermal cells radiating from the tubercle (arrowed). E, Seed scar in oblique view showing the mound-like tubercle and radiating files of epidermal cells (arrowed). Scale bars ¼ 1 mm.

Nevertheless, since we recognize homologous charac- bract (Plumstead 1952; Fig. 7B), radially symmetrical ters among the reproductive structures of all glossop- strobili bearing many pollen sacs (Banerjee 1973)or terid families, the following discussion is relevant to seeds with elongate projections (Walton in Plumstead the fructifications of the entire order. Scutiform glos- 1952; Fig. 7C), strobili with especially prominent seed- sopterid fructifications have been interpreted variously bearing scales (Surange & Maheshwari 1970; Fig. 7E), as bi-valvate structures consisting of either a sterile radially symmetrical cones occurring in isolation or bract or microsporophyll and an opposing megasporo- subtended by a sterile bract (Surange & Chandra phyll (Plumstead 1952, 1956a; Fig. 7A, D, G), fleshy 1973a, 1975, White 1986; Fig. 7F), radially symmet- structures embedded in a leaf surface and covered by a rical receptacles surrounded at the base by a peltate 488 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Fig. 7. Illustrations of some of the divergent interpretations of glossopterid polysperm and fertiliger architectures proposed since the 1950s. A, Bivalvate and bisexual model proposed for Scutum by Plumstead (1952, 1956a) showing (i) hypothesized pollen-bearing and ovuliferous halves, ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 489

Fig. 7 (Continued) (ii) cupule fusion after pollination, and (iii) polleniferous bracts (in reality winged seeds) attached to the fertile surface of the receptacle. B, Model preferred by Plumstead (1952) for ‘Lanceolatus’ proposing fusion of the polysperm and leaf to form an enclosed ovuliferous compartment; C, Model preferred by Walton in Plumstead (1952) for Scutum inferring (i) radial symmetry with (ii) ovules or sporangia bearing tubular appendages. D, Model proposed by Plumstead (1958a) for ‘Hirsutum’ suggesting separate (i) ovuliferous and (ii) polleniferous halves, the latter shedding upswept, hair-like pollen-bearing structures to yield (iii) an empty cupule on maturity. E, Model preferred by Surange & Maheshwari (1970) for Scutum with (i) ovules borne on flattened scales arranged on (ii) a radially symmetrical strobilus. F, Model preferred by Surange & Chandra (1975) for Scutum showing (i) inferred bivalvate architecture of polysperm that is (ii) lensoid and surrounded on all sides by ovules. G, Model preferred by Plumstead (1956b) for Ottokaria showing (i) the inferred veined half, and (ii) fertile half of a (iii) bivalvate polysperm. H, Model preferred by Surange & Chandra (1975) for Ottokaria showing (i) inferred peltate bract subtending (ii) a radially symmetrical ovuliferous ‘head’. I, Model preferred by Banerjee (1978) for Ottokaria showing (i) the compacted appearance of the polysperm inferred to consist of (ii) separate sterile bract and branched, filamentous, ovuliferous portions. J, Model proposed by Nishida et al.(2018) for lidgettonioid fertiligers with ovules inferred to be positioned adaxially but facing the subtending leaf on recurved polysperms. K, Model preferred by Maheshwari (1965), Schopf (1976) and Gould & Delevoryas (1977) for scutiform fructifications consisting of a dorsiventral polysperm borne in the axil of a leaf but adnate to the lower portion of a subtending leaf and having (i) an ovuliferous abaxial surface and (ii) a veined adaxial surface. L, Models developed by Adendorff et al.(2002), Prevec et al.(2008) and Prevec (2014) for three genera of bi-winged scutiform polysperms: (i) Gladiopomum (with secondary wing reduced to an apical spine), (ii) Bifariala (with closely superimposed primary and secondary wings), and (ii) Elatra (with a hooded primary wing and distally expanded secondary wing). bract (Surange & Chandra 1975, Rigby 1978; Fig. 7H), organs attributed to Scutum (Fig. 1B) were more or branched ovuliferous filaments covered by a protective less flattened bivalvate structures with a sterile bract bract (Banerjee 1978; Fig. 7I), or bilaterally symmet- covering a winged fertile receptacle bearing numerous rical, dorsiventral capitula or cupules with seed-bearing sac-like structures that may have represented ovules surfaces facing away from (Pant & Nautiyal 1984), (Fig. 7A). Plumstead’s(1952) paper contained an adaxial but recurved towards (Fig. 7J) or abaxially appendix with commentaries on the fructification archi- positioned and facing towards (Fig. 7K) the subtending tecture by some of the foremost palaeobotanists of that leaf (Schopf 1976, Gould & Delevoryas 1977, time. These commentaries reveal that, from the earliest Anderson & Anderson 1985, McLoughlin 1990b, 1995, serious investigations of these fossils, markedly diver- 2011b, Prevec et al. 2008, Prevec 2011, Nishida et al. gent interpretations on the structure and relationships of 2018). Whether the seeds were borne on the abaxial these organs were developed. A few of the commenta- surface of the fructification (facing the subtending ries are especially noteworthy. leaf), the adaxial surface (facing away from the leaf), John Walton (in discussion of Plumstead 1952) pro- or on both, has raised particular controversy owing to posed that the scutiform seed-bearing organ was actu- contrasting inferences drawn from adpression and per- ally cone-like or radially symmetrical and that each mineralized fossils (Maheshwari 1965, Pant & Nautiyal seed bore a long, tubular appendage. He envisaged 1984, McLoughlin 1990b, 1995, 2011b, Taylor & that, when compressed, these appendages would over- Taylor 1992, Nishida et al. 2007, Prevec et al. 2008, lap along the periphery of the fructification to produce Prevec 2011, 2014). Moreover, Doyle (2006) has a wing-like feature on impressions (Fig. 7C). Tubular ‘ ’ argued that the lower surface of the megasporophyll appendages over the central part of the receptacle might be structurally adaxial if attached to a dormant would be compressed end-on to create an imprint with axillary bud that is adnate to the subtending leaf. The indistinct vein-like grooves that Plumstead (1952) had contrasting interpretations presented for the structure of interpreted as the ‘empty’ half of a cupule, or what we glossopterid fructifications appear to have arisen in interpret to be the ‘back’ or ‘ovule-free side’ of a seed- large part from the difficulties in conceptualizing the bearing organ, showing venation (Fig. 7A). Walton lik- original three-dimensional shapes of organs preserved ened the general morphology of the fructifications to variably as impressions, compressions or siliceous per- Lepidostrobus (lycophyte) strobili. Later, Surange & mineralizations. We explore these issues in the sections Maheshwari (1970) favoured Walton’s interpretation below and note that accurate reconstruction of fructifi- except that they considered the seeds to have been cation architecture is essential for correctly coding the borne on flattened, scale-like structures that were espe- characters of glossopterids in phylogenetic analyses of cially prominent at the margins of one plane through seed plants. the fructification (Fig. 7E). Wilfred Norman Edwards in discussion of Plumstead’s(1952) article also sug- Receptacle symmetry gested that the fructifications were ‘cone-like’ but Most controversy has focused on interpreting the struc- offered no further detailed assessment of ture of multiovulate scutiform (¼dictyopteridioid) glos- their morphology. sopterid ovuliferous organs. Plumstead’s(1952) study Several subsequent authors favoured a strobilar of glossopterid reproductive organs from South Africa interpretation of glossopterid fructifications but with provided the first serious evaluation of fructification slight modifications in some cases. It is possible that morphology, and the first examples of polysperms in many authors inferred radial symmetry for glossopterid clear attachment to a subtending leaf. She argued that fructifications (Fig. 7C, E, H) influenced by a desire to 490 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA find similarities with extant cycad, conifer, gnetalean, Dictyopteridium, which they regarded as radially or angiosperm reproductive structures. For example, symmetrical. The idea that the receptacle was fleshy, Melville (1983b, fig. 1f) envisaged scutiform glossop- appears to have arisen from the interpretation of the terid fructifications to consist of a dish-shaped scale narrow fluted wing as a laterally compressed rank of (scutella) supporting an epiphyllous, spike-like group marginal ovules. Rigby (1978) argued that the of branches more or less adnate to one another and receptacles of both Scutum and Dictyopteridium were bearing terminal ovules. He referred to the subtending essentially ovoid to cylindrical with two longitudinal glossopterid leaf as a bract by analogy with an angio- planes of symmetry (180 rotational symmetry). sperm bract and flower. He interpreted the fossil Despite these various interpretations favouring Breytenia plumsteadiae Melville, 1983a as a cluster of cylindrical, conical, lensoidal or in some way a thick- ovule-bearing branches enclosed by an urn-shaped ened fleshy structure for glossopterid fructifications, structure formed by the enrolling of an attached scale. other authors found no evidence to support these He used analogies with extant flowering plants to sup- hypotheses (Fig. 7G, J–L). For instance, Tom Harris, in port his hypothesis that angiosperm flowers were discussion of Plumstead’s(1952) paper, proposed that derived from glossopterid fructifications. the ‘empty half’ of organs attributed to ‘Lanceolatus’ Rigby (1972b) interpreted radial symmetry in (Fig. 7B) might simply represent the sterile back Dictyopteridium, inferring tubercles arranged around a (veined surface) of the ‘fertile half’, and that features cylindrical axis that appeared to lack a marginal wing. originally described as ‘burst sacs’ might constitute the Although identical in size, shape and seed-scar morph- scars of detached seeds. Hughes (in Plumstead 1956b, ology, Rigby (1972b) inferred Dictyopteridium to be a p. 224) concurred with Harris’ interpretation, and com- more or less cylindrical organ and distinct from mented that the fossils appeared to be typical impres- Isodictyopteridium, which he interpreted to be laminar. sions in which the carbonized organic matter had been The specimen assigned to ‘Fructification cf. destroyed, leaving a small air space between part and Dictyopteridium sp.’ by Rigby (1972b, text-fig. G), counterpart. In the case of Plumstead’s(1952) fossils which was the principle basis for his interpretation of from Vereeniging, South Africa, Hughes inferred that radial symmetry, can be reinterpreted to represent a the space would then represent the void left by a sim- longitudinally folded, dorsiventral organ. That specimen ple flattened organ with a veined abaxial and a seed- bears seed scars along only the left margin (that area bearing adaxial surface (Fig. 8A–H). representing the receptacle), whereas the portion on the Most early research had been carried out on impres- right of the organ constitutes a transversely striate sion fossils but, on the basis of a Canada balsam trans- wing. On this basis, Dictyopteridium and fer preparation from a coalified compression in India, Isodictyopteridium appear to be synonymous. Maheshwari (1965) argued that Dictyopteridium was a Surange & Chandra (1973a) also inferred radial flattened dorsiventral organ with ovule attachments symmetry for seed-bearing examples of restricted to one surface and venation evident on the Dictyopteridium. Later, they maintained their interpret- other—features consistent with Harris’ (in Plumstead ation of radial symmetry for Dictyopteridium (Surange 1952) earlier interpretation. Various other early authors, & Chandra 1974, 1975, Chandra & Surange 1976) but even investigating impression fossils, also concluded proposed bilateral symmetry (albeit with a thickened that ovules or seed scars were restricted to one surface receptacle that was inferred to be lenticular in cross- of the polysperm; the reverse surface revealing only section) for morphologically similar organs attributed venation and implying a dorsiventral character with to Scutum (Fig. 7F). Surange & Chandra (1975) sug- bilateral symmetry (i.e., a single plane of symmetry: gested that the seeds of Senotheca (Figs 1D, 5I) were Pant & Nautiyal 1965, 1966, 1984, Banerjee 1968, inserted spirally around a linear receptacle, the distinct Rigby 1972b, Schopf 1976). Thin-sectioning of permin- flanges on either side of the compressed receptacle rep- eralized remains later confirmed a bilaterally symmet- resenting ranks of overlapping seeds. They further con- rical, dorsiventral organization for scutiform sidered Ottokaria (Fig. 1C) to represent a radially polysperms (Gould & Delevoryas 1977). symmetrical strobilus surrounded by a circlet of par- Despite the convincing anatomy of the permineral- tially fused bracts (Fig. 7H)—a model also favoured by ized fertile organs, Rex’s(1986) experimental model- Rigby (1978). Chandra & Surange (1977a) also fav- ling of adpression fossils using artificial materials oured radial symmetry for the receptacle of another failed to find support for the architecture outlined by scutiform fructification, Venustostrobus indicus. Gould & Delevoryas (1977). Rex (1986) apparently Somewhat ambiguously, Lacey et al.(1975) indi- mistook Plumstead’s(1952) fossils for casts (positive cated that multiovulate fructifications assigned to replicas) rather than moulds (negative imprints). Plumsteadia from the Lopingian Normandien Consequently, her attempts to model the original shape Formation (formerly the Estcourt Formation), South of glossopterid ovuliferous organs through artificial Africa, were bifacial organs, perhaps with a somewhat compressions gave spurious results favouring a cone- fleshy receptacle but otherwise similar to like architecture. A dorsiventral, laminar morphology ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 491

Fig. 8. Models of scutiform glossopterid polysperms and fertiligers showing the generation of contrasting moulds of the ‘fertile’ surface from which the seeds have been shed (tubercles representing points of seed detachment) and the ‘sterile’ (veined) surface (adapted from Prevec 2011). A, Reconstruction of the seed-scar-bearing surface of a typical scutiform glossopterid polysperm. B, Polysperm reconstruction (A) colour coded to show the main architectural components and the line of a hypothetical cross-section in C and D. C, Cross-section of polysperm compression buried in the rock matrix. D, Cross-section of rock fractured through the mould of a polysperm showing separated veined (sterile) surface impression (top) and tuberculate (seed-scar-bearing) surface impression (bottom). E, Reconstruction of a fertiliger incorporating a scutiform polysperm viewed from the upper (adaxial surface). F, Polysperm colour coded to show the main architectural components and the line of a hypothetical cross-section in G and H. G, Cross-section of the colour-coded polysperm and subtending leaf compressions buried in the rock matrix (with seeds borne abaxially—facing the leaf). H, Cross-section of rock fractured through the mould of the fertiliger showing separated veined (sterile) surface impression (top) and tuberculate (seed-scar-bearing) surface impression (bottom) on a wedge of sedimentary matrix that typically adheres to the mould of the underlying leaf by a thin veneer of clays or mineral cements. for scutiform glossopterid fructifications has been reaf- Ryberg 2010, Ryberg & Taylor 2013, McLoughlin firmed by subsequent studies of permineralized ovulif- et al. 2019), and also of impression fossils from vari- erous organs from Australia and Antarctica (Taylor & ous regions (McLoughlin 1990a, Prevec et al. 2008, Taylor 1992, Pigg & Trivett 1994, Nishida et al. 2007, Prevec 2011, 2014). 492 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Bipartite architecture, the presence of a protective fructifications, Norman Hughes also disputed the bract and gender bipartite character of the fossils and favoured a simple (single-part) dorsiventral organization. A two-part or valvate architecture, or the presence of a Plumstead (1956a) later presented a modified inter- separate sterile bract protecting the seed-bearing surface pretation of the South African fructifications, and iden- of the polysperm was a common interpretation by early tified overlapping bract-like and hair-like features in researchers of glossopterids. Plumstead (1952) errone- some of the impressions, interpreting these as elongate ously interpreted Scutum fructifications from staminate organs attached to the normally sterile half of Vereeniging, South Africa, as compressions or casts the ‘cupule’ (Fig. 7Aiii, Dii, iii). Plumstead (1956a) and inferred that the part and counterpart of the fossils argued that the fructifications represented bisexual (in reality impressions and, therefore, two halves of a cupules and, thus, were angiosperm-like in their struc- single flattened mould) represented two valves of a bilaterally symmetrical ‘cupule’. She interpreted one ture and affinities. The bract-like features reported by half of the ‘cupule’ (closest to the subtending leaf) to Plumstead (1956a) were regarded by Surange & — be a fleshy, fertile head bearing embedded oval ‘sacs’ Chandra (1974) as elongate wings of attached seeds on the inner surface; the outer surface showing only an interpretation supported here, although we consider venation and a ‘raised and roughened central portion’ the seeds to have been attached to one side of a dorsi- (Fig. 7A). The entire head was regarded as being ventral fructification. The hair-like pollenate features fringed by a sterile wing. She interpreted each sac-like described by Plumstead (1958)inHirsutum were later raised feature on the fertile head to contain a seed. demonstrated by Anderson & Anderson (1985)tobe Surange & Maheshwari (1970), Surange & Chandra upswept striations on the marginal wing, the full impli- (1974) and Rigby (1978) also mistakenly interpreted cations of which we discuss below. Plumstead (1956b) ‘ ’ similar fructifications to be preserved as casts rather proposed that the two cupule valves of Ottokaria than impressions and likewise interpreted the raised became fused in later stages of growth to produce a mounds on specimens of Plumsteadia and Scutum to single, bilaterally symmetrical structure. In discussion ’ represent seeds, rather than depressions on the original of Plumstead s(1956b) paper, Tom Harris astutely plant surface. Plumstead (1956a), Surange & questioned her interpretation of the two-part structure ‘ ’ Maheshwari (1970) and Rigby (1978) interpreted the of the fructifications, the stigmas , and the nature of ‘ ’ tubercle on each raised mound to represent a stigmatic the male bracts . These features have subsequently surface or micropyle—in reality it represents the vascu- been interpreted, respectively, as a single flattened lar trace of a seed scar. organ, tuberculate seed scar moulds, and as the veined, Plumstead (1952) regarded the counterpart of typ- seedless surface of the laminar polysperm (dis- ical Scutum fossils, and later (Plumstead 1956b)of cussed below). Ottokaria specimens, to represent the sterile, concave Plumstead (1958) re-emphasized her interpretation half of a ‘cupule’ showing only venation patterns on of the bipartite ‘cupules’ of glossopterid fructifications both surfaces, it too being fringed by a striate wing. with the description of additional South African She adopted a similar interpretation for fructifications impression fossils. However, she departed from this that she assigned to Lanceolatus (later considered syn- scheme by interpreting specimens of Pluma (considered onymous with Plumsteadia; see Rigby 1978), but with here to represent laterally compressed specimens of some minor modifications. ‘Lanceolatus’ was inter- Scutum) as representing separate ovuliferous and stam- preted as a structure consisting of: (1) a fertile head inate, single-part, dorsiventral organs. that was embedded within the tissue of a leaf; and (2) Rigby (1963), following Plumstead’s earlier model, a sterile half of a ‘cupule’, the margins of which upon also interpreted Plumsteadia microsacca as a bipartite maturity fused with the tissues of the leaf to form an organ but with a non-saccate, ‘sterile organ’ adnate to enclosed structure covering the fertile head (Fig. 7B). the subtending leaf and a free, fertile, ‘sac-bearing’ She further suggested that the seeds of ‘Lanceolatus’ receptacle with sacs facing the sterile organ. He later were represented by small, flat discs that were shed (Rigby 1978) reinterpreted the fructifications of from the cushioned surface of the fructification on Plumsteadia to lack the protective bract invoked for maturity. Plumstead concluded her 1952 paper with ref- other genera by Plumstead (1952) and argued that the erence to the angiosperm-like properties of these appar- bract was, at least in the case of P. microsacca, a pres- ently bipartite, cupulate fructifications. ervational artefact caused by flexure of the overlapping In the appendix of Plumstead’s(1952) article, Tom portion of the subtending leaf around the compressed Harris was sceptical (or perhaps cynical: see Schopf fructification during burial. 1976, p. 28) of the bipartite, cupulate interpretation of White (1964) interpreted Plumsteadia ampla to be a the fructifications and suggested that the sterile and fer- radially symmetrical cone-like structure covered on one tile halves of the fossil were merely part and counter- side by a bract. Surange & Maheshwari (1970) also part of a single, dorsiventral organ. In the discussion of favoured a cone-like structure for Plumsteadia pretiosa Plumstead’s(1956b) later description of Ottokaria but did not find evidence for a protective bract. Rather, ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 493 they surmised that the counterpart showed an irregular, the midribs of Glossopteris leaves. He interpreted venation-like patterning caused by imprints of elongate these, respectively, as the ovuliferous and microsporan- scales (seed-bearing structures) borne on the receptacle. giate fructifications of Austroglossa walkomii, which Surange & Chandra (1973a) initially found no evi- implied that the fructifications had either a bipartite dence of a bract covering the receptacle of structure or were borne on separate leaves. However, Dictyopteridium but, later (Surange & Chandra 1974, Holmes (1990) later indicated that both organs repre- 1975, Chandra & Surange 1976), inferred the presence sented dorsiventral ovuliferous fructifications com- of a close-fitting, protective, multiveined bract attached pressed in different orientations either with or without to various scutiform glossopterid fructifications includ- attached seeds. ing Dictyopteridium. Of particular note, Chandra & Despite these numerous interpretations favouring a Surange (1977a) inferred the presence of a protective bipartite structure, and/or microsporangiate component bract covering the receptacle of Venustostrobus indicus to scutiform glossopterid fructifications, some authors (¼Scutum indicum) based on the recovery of cuticle studying adpression fossils (e.g., Maheshwari 1965, from a cellulose acetate peel of the fructification Pant & Nautiyal 1965, 1966, 1984, Schopf 1976) main- following removal of the seeds on a previous peel. tained that these were unipartite organs with ovules or Their ‘bract’ is considered here to represent a misinter- seed scars restricted to one surface; the reverse surface pretation of the veined surface of a dorsiventral revealing only venation and implying a dorsiventral fructification, with the ‘bract cuticle’ probably deriving character with bilateral symmetry. This interpretation from either the sterile surface of a dorsiventral fructifi- was ultimately confirmed by the discovery of anatomic- cation or from an unrelated underlying leaf. ally preserved (permineralized) fructifications in Srivastava (1978) favoured the earlier interpreta- Australia having a leaf-like architecture with thin tions by Surange & Chandra (1975) and inferred the enrolled margins (wings) partially enclosing the ovules presence of a dentate bract overlying the receptacle of borne on one surface of the organ (Gould & Ottokaria biharensis. Srivastava (1978) interpreted the Delevoryas 1977; Fig. 9A). only available specimen of this species to be preserved Subsequent authors have shown, diagrammatically, partially as a cast and partially as a mould. The illus- how fossils can yield different morphologies of the trated specimen appears to represent simply the part fructifications depending on whether compressions or and counterpart of an impression. In interpreting impressions (moulds) are available, and where the Ottokaria raniganjensis, Banerjee (1978) favoured plane of fracturing passes through the organ Plumstead’s two-part model but suggested that the (McLoughlin 1990a, 1990b, Prevec et al. 2008, Prevec lobed bract covered a fertile part consisting of finely 2011, 2014). Additional permineralized fructifications forked peduncles bearing terminal seeds (Fig. 7I). from Australia and Antarctica have confirmed that a Other authors favouring a bipartite structure include single-part, laminar morphology with ovules attached to one surface is a consistent architectural style among Benecke (1976), who emended the diagnosis of glossopterid fructifications (Taylor & Taylor 1992, Dictyopteridium to include the presence of a sterile Pigg & Trivett 1994, Nishida et al. 2007, Ryberg 2010, protective bract. White (1986) also reconstructed many Ryberg & Taylor 2013, McLoughlin et al. 2019). A ovuliferous organs to be radially symmetrical cones cone-like (strobilar) arrangement is now dismissed for with either a protective bract on one side or forming a all glossopterid fructifications. All scutiform (dictyop- broad sheath at the base. Banerjee (1984) considered teridioid), flabellate (rigbyoid), cupulate (lidgettonioid) the dorsiventral receptacle of multiovulate, scutiform, and branched (arberioid) fructifications are interpreted glossopterid fructifications to be covered on the ovulif- here as ovule-bearing organs. erous side by a scale-like bract. She suggested that another fossil, assigned to Bankolaea, represented a cone-like organ enclosed by bracts but these fossils Seed-scar morphology appear to represent scale-leaves bearing pollen sacs Most fossils of glossopterid polysperms lack attached (microsporophylls). seeds. Normally, seeds were shed at maturity before The notion that some scutiform glossopterid organs dehiscence of the polysperm. In a few cases, apparently were microsporangiate rather than ovuliferous has mature seeds are retained on the detached polysperm emerged repeatedly, with Dictyopteridium (or (Holmes 1974, Prevec 2014) and anemochory via shed- Isodictyopteridium) being commonly inferred to be a ding of the whole reproductive organ may have been a pollen-bearing organ (Rigby 1972b, Anderson & successful dispersal strategy. In some cases where large Anderson 1985). Banerjee (1973) argued that numbers of small co-preserved polysperms retain Dictyopteridium was a microsporangiate cone-like attached ovules/seeds (e.g., Gould & Delevoryas 1977, organ covered by a scale leaf of equal dimensions. Nishida et al. 2007), the fructification may have been Kyle (1974) also inferred the raised features on aborted prematurely or detached from the parent plant Plumsteadia to be hollow, pollen-bearing sacs. Holmes by physical damage before reaching maturity. In the (1974) illustrated stub-like and ovate organs attached to case of mature polysperms, seed detachment typically 494 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Fig. 9. Anatomy of permineralized glossopterid polysperms. A, Transverse section through a specimen of Homevaleia gouldii Nishida et al., 2007 showing single-layered epidermis, adaxial mesophyll layer of large elliptical cells, sparse veins, abaxial laminar mesophyll layer of brick- like cells, and thin marginal wings wrapping around abaxial ovules during early development; un-numbered specimen of Gould & Delevoryas (1977) illustrated in inverted orientation by Nishida et al., (2007, fig. 1e). B, Line drawing of a portion of a transverse section through a specimen of Homevaleia gouldii showing mesophyll structure (opaque fillings of cells excluded) and vascular bundle apparently consisting of a few central xylem tracheids surrounded by thin-walled phloem cells; UNEF15286. C, Line drawing of a portion of an oblique to longitudinal section of a Homevaleia gouldii polysperm showing mesophyll structure and indistinct vasculature; UNEF15285. D, Line drawing of a transverse section through the holotype of Lakkosia kerasata Ryberg, 2010, a possible rigbyoid polysperm, showing thin marginal wings partially wrapping around ovules attached to abaxial surface of receptacle; KU slide 7837 (13676 D-bot series d peel 59). E, Enlargement of a portion of D showing ambiguous anatomy of vasculature. Abbreviations: Ov ¼ ovule, W ¼ wing, V ¼ vein, Xy ¼ xylem, Ph ¼ phloem, PhL ¼ putative phloem lacuna, RM ¼ robust mesophyll layer of large cells, LM ¼ laminar mesophyll layer of small brick-shaped cells. Scale bars ¼ 1 mm for A, D; 100 mm for B, C, E. ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 495 left behind distinctive scars on the receptacle (Fig. (Fig. 5P) has consistently small and pitted seed scars in 5A–S). These are best expressed in impression fossils contrast to the broad platform-like scars of Nogoa (Fig. and can be represented by either depressions (Figs 5H, 5Q). Within Dictyopteridiaceae, the diminutive, well- J, 6A, B, D, E; Tewari et al. 2012) or, more com- spaced seed scars of Dictyopteridium (Fig. 5A) readily monly, raised mound- or platform-like (i.e., cushion- differentiate this genus from forms attributed to like) structures (Fig. 5D, E, G, L). In other cases, the Plumsteadia, which have crowded and bulbous seed scars are subtle and difficult to detect (Fig. 5B, I, M, scars (Fig. 5E, G). In the absence of preserved ovules, O, R). Inverting the (negative) features preserved on the detachment scars are also useful for inferring the impressions (Fig. 6B) provides an image of the (posi- number of seeds borne on the diverse range of poly- tive) features of the original organs (Fig. 6C). sperms. This information is important in relation to As indicated in the previous sections, the raised hypothesized reduction series that have inferred deriv- scars of some polysperms have been interpreted as pol- ation of angiosperm carpels from glossopterid fertil- len sacs by some workers. This interpretation has been igers (Retallack & Dilcher 1981). promoted on the basis that some of the raised structures appear to be hollow (Plumstead 1952, Banerjee 1973). Wing morphology However, McLoughlin (1990b, pl. 1, fig. 3) showed The nature of the marginal wing around glossopterid that these inferences were the result of incorrect inter- polysperms has provoked contrasting opinions since the pretation of the polysperms as casts rather than impres- early 1950s. Plumstead (1952) identified a fluted, sions, and that the empty ‘sacs’ actually represent apparently membranous, sterile flange of tissue around cavities left by decayed seeds that were attached to, Scutum fructifications from the Karoo Basin—a feature and underlie, the mould of the receptacle. Seed scars that, in the discussion of that paper, JohnWalton argued are generally small (<1 mm in diameter; e.g., to represent a series of overlapping seed-borne tubular Fig. 5A–D) and packed tightly on glossopterid poly- appendages (Fig. 7C). Although the wing (usually per- sperms but, in a few cases (e.g., Fig. 5Q, S), they are ceived as a thin, marginal, sterile extension of the isolated and reach up to 5 mm in diameter suggesting receptacle) has been deemed an integral part of the that different taxa supported seeds of strongly contrast- ovuliferous receptacle by many authors (see ing size. McLoughlin 2011b), the notion that it represents a ser- The tubercle or pit typically preserved in the centre ies of marginal seeds or their flanged extensions has – – of each seed scar (Figs 5A, C H, P, 6A E) undoubt- appeared repeatedly in the literature. For example, edly represents the position of the vascular supply to Rigby (1978) suggested that the wing in Scutum and the seeds, as permineralized specimens reveal attach- Dictyopteridium represented a marginal row of abut- ment of the seeds by either a short pedicel (McManus ting, winged ovules. Surange & Chandra (1974) inter- et al. 2002, Nishida et al. 2007, McLoughlin et al. preted the wing of Scutum sahnii as a sterile flange of 2019) or depression (Ryberg 2010, McLoughlin et al. tissue, but those of Scutum elongatum and S. indicum 2018) supplied by a single central vascular strand. It to have been formed by a marginal row of overlapping, should be noted that the tubercles on the mould flattened seeds. They favoured this latter interpretation (impression fossil) of a seed scar (Fig. 6B) correspond for the wings for Scutum and Senotheca species in a to a depression on the original receptacle (Fig. 6C). later treatment of Indian fructifications (Surange & The presence of prominent radial striae (Fig. 6D, E; Chandra 1975). Ryberg 2009) or hairs on or between the seed scars has Additional models have been proposed for the been noted in several studies (Ryberg 2010, Prevec nature of the wings that are variants on these previous 2014), and these may relate in some way to protection schemes. Plumstead (1958) proposed that the wing of of the ovules. In the case of Homevaleia, a complex Scutum thomasii Plumstead, 1958 was thick and fleshy network of multicellular filaments fills the spaces in life rather than membranous. Surange & Maheshwari between the developing ovules (Nishida et al. 2007, (1970) interpreted the wing of Plumsteadia pretiosa to fig. 6). Gould & Delevoryas (1977) hypothesized that be composed of a series of lateral scales, each with an these structures might have functioned in some way to ovule borne at the base. aid the pollen-drop mechanism in directing pollen In some cases, scutiform (¼Dictyopteridiaceae) towards the micropyle, whereas Nishida et al.(2007) fructifications have been interpreted to lack a marginal suggested that the meshwork might have helped to wing entirely. The original and first revised diagnoses insulate the ovules in a cool temperate climate. of Plumsteadia (Rigby 1963, 1971) indicated the Regardless of their structural interpretations, the absence of a marginal wing. Lacey et al. (1975) also varied morphologies of the seed scars (Fig. 5A–S) and interpreted Plumsteadia natalensis to lack a true wing, their relative consistency within individual populations the wing-like marginal rim purportedly being formed (Prevec 2011), suggest that these features may be par- by contiguous marginal ‘sacs’; Anderson & Anderson ticularly useful in segregating taxa at specific and gen- (1985) referred to this feature in both ‘Lanceolatus’ eric ranks. For example, within Rigbyaceae, Rigbya and Plumsteadia as a ‘rank of modified ovules’. 496 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Nevertheless, a narrow flange identical to the wings of (Figs 3A–D, 7Lii). The double-winged structure is other representatives of Dictyopteridiaceae is evident in unlike that of most other glossopterid fertile organs, many specimens of P. natalensis, and in the holotype but homologies were also noted between the distally of the type species of the genus (P. microsacca: Rigby extended ‘secondary’ wing of Bifariala and the spine- 1978, fig. 4). Plumstead (1952) similarly declared the like apical extension of the receptacle in Gladiopomum absence of a marginal wing in organs attributed to (Fig. 7Li, ii; Adendorff et al. 2002, Prevec et al. 2008). ‘Lanceolatus’, and considered the narrow, fluted An even more elaborate architecture was detected in regions along the periphery (here interpreted as por- Elatra Appert, 1977 (Fig. 1H), which, like Bifariala, tions of a wing) to be remnants of an overlying ‘sterile has two superposed wings (Figs 4A–F, 7Liii). One of bract’. Chandra & Surange (1977b) dismissed the pres- these is acuminate, has campylodromous venation, is ence of a wing in their description of confluent with the veined surface of the fructification, Plumsteadiostrobus. Nevertheless, a narrow fluted and is homologous with the ‘secondary wing’ of flange is evident around their illustrated specimens, and Bifariala (Prevec 2014). The other wing is radially stri- similar slender wings have been noted on other ate and contiguous with the seed-bearing surface of the Plumsteadia-orDictyopteridium-type fructifications receptacle (i.e., homologous to the ‘primary wing’ of (Maheshwari 1965, Benecke 1976, McLoughlin Bifariala). In the basal portion of Elatra, this wing is 1990b). Further, although Holmes (1974) originally similar to the solitary wing of Scutum but, distally, this described Austroglossa walkomii fructifications as con- wing arches to form a hood-like structure that partially sisting of a spindle-shaped, wingless receptacle, he later covers the ovuliferous surface (Prevec 2014). Atypical recognized that the fructifications were dorsiventral arching of the striae and an unconventional wing orien- organs based on additional specimens that were not tation with respect to the receptacle in other fructifica- compressed laterally, and that these specimens bore a tions, such as Ottokaria sp. of White (1978) and narrow fluted marginal wing (Holmes 1990, pl. 1, Karingbalia McLoughlin, 2016, suggest that additional fig. 9). novel wing architectures are likely to be found among Confidence in the presence of a marginal wing con- glossopterid ovuliferous organs in the future. tiguous with a flattened receptacle and free of seed The contiguous striate wing segments of attachments was advanced when Gould & Delevoryas Dictyopteridiaceae and Lidgettoniaceae polysperms may (1977) identified a thinned marginal flange around the have derived from lateral amalgamation of the flanges receptacle in anatomically preserved (permineralized) flanking the seed-bearing branches of Arberiaceae and polysperms (Fig. 9A), although Taylor & Taylor (2009) Rigbyaceae fructifications. In turn, these flanges may remained sceptical that this marginal extension would represent the vestiges of individual megasporophylls form a wing on compressed specimens. Subsequent that were mostly lost in glossopterid fructifications through an evolutionary process of planation and con- studies of permineralized taxa have confirmed that the densation of the polysperm from what was originally a wings of most taxa are simple thinned extensions of radially symmetrical axillary fertile shoot. the receptacle that arch over the ovuliferous surface during early development (Nishida et al. 2007, Ryberg 2010, Ryberg & Taylor 2013). Orientation of the ovuliferous surface Despite permineralized remains clarifying the struc- Many glossopterid polysperms referable to various gen- ture of the wing in typical scutiform polysperms, cer- era from sites throughout Gondwana have been found tain fructifications preserved as impressions continued attached to a subtending leaf. Consequently, the pos- to reveal novel features. Plumstead (1956a) noted an ition of the ovules on the receptacle, and their orienta- apparent fringe of upswept hairs overlapping a narrow tions with respect to the subtending leaf ought to be continuous wing in ‘Hirsutum dutoitides’ (Fig. 7D). readily apparent. However, the adaxial versus abaxial These overlapping features were probably responsible insertion of the ovules on the laminar receptacle has for her claims that glossopterid fructifications were been one of the major and persistent points of dispute bipartite cupules composed initially of tightly appressed concerning fertiliger architecture (Fig. 10A–C). and similar-shaped valves, which opened to expose Plumstead (1956a) provided a reconstruction of Scutum ovules on one half and filamentous pollenate organs on with the seed-bearing surface of the ‘cupule’ facing the other (Fig. 7Di–iii). Careful degagement of succes- away from the subtending leaf (Fig. 7A). However, sive claystone laminae hosting the structures fringing other authors (e.g., Schopf 1976) maintained that the the receptacle on these specimens enabled Prevec et al. fertile surface of the receptacle faced towards the sub- (2008) to identify a double-winged organization of tending leaf (Fig. 7K). Again, taphonomic artefacts and these fructifications and establish the new genus diverse preservational styles contributed to these diver- Bifariala (Fig. 1G). One wing has rounded basal lobes gent interpretations. and is radially fluted and striated, as is typical of scuti- Plumstead (1958, pl. 23, fig. 1) figured an example form fructifications, whereas the other has an extended of Pluma longicaulis (¼Scutum leslii) interpreted to be apex and bears fine striae that markedly curve distally attached to a Glossopteris leaf. The ovuliferous surface ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 497

Fig. 10. Contrasting interpretations of the orientation of seeds on the polysperms of glossopterids. A, Seeds orientated adaxially on a megasporophyll based primarily on interpretations of the leaf-like vasculature of the polysperm (Taylor & Taylor 1992). B, Seeds directed ventrally, but structurally adaxial with respect to a dormant axillary shoot adnate to the subtending leaf (sensu Doyle 2006). C, Seeds orientated abaxially on a fertile cladode (this study) based primarily on modelling of fertiligers preserved as moulds and on the presence of abaxial xylem in some conifer ovuliferous scales. D, Schematic of longitudinal section through an ovuliferous cone of Pinus maritima, modified from Aase (1915). E, Enlargement of base of cone, illustrating the changes within the bract/scale complex, from a dominant bract and reduced ovuliferous scale in the basal-most complexes, to a dominant ovuliferous scale and highly reduced bract in the seed-bearing portion of the cone. Stippled fill ¼ shoot/strobilar axis. Empty fill ¼ leaf. Horizontal lined fill ¼ axillary shoot/cladode. of this laterally flattened fructification faces away from a mould, the fertile surface of the fructification faces the the leaf. However, the connection between the fructifi- subtending leaf. Rigby (1978) similarly interpreted cation and leaf is equivocal and probably does not rep- Plumsteadia microsacca to have ovules inserted on the resent a life-like arrangement. surface of the fructification facing away from the Lacey et al. (1975) considered the ‘sac-bearing’ attached leaf based on the position of raised seed scars. (ovuliferous) surface of Plumsteadia fructifications to However, he failed to recognize that the tubercles repre- be oriented away from the attached leaf; however, they sented the negative image (mould) of the original fertile incorrectly interpreted the fructifications to represent face of the fructification; hence, the orientation of the casts rather than impressions, and when reinterpreted as seeds with respect to the leaf ought to be inverted. 498 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

to be adaxial—an arrangement that they maintained was generated by 180 recurvature of the polysperm pedicel such that the apical end of the polysperm pointed towards the leaf base (Fig. 7J). However, we find no evidence from the illustrated specimens (Nishida et al. 2018, figs 8.1–8.12) that these poly- sperms were recurved and, instead, interpret the puta- tively attached longitudinal section of a megasporophyll to be a transverse section of an enrolled polysperm abutting the subtending leaf. Gould & Delevoryas (1977), in their seminal paper describing the first permineralized glossopterid fructifications to be sectioned, explained how the ‘overlapping part of the megasporophyll generally faces the associated Glossopteris leaf (palisade or adaxial side) when one is present’, although they did not provide photographic evidence to this effect. Their study showed that the receptacle of Homevaleia was composed primarily of a uniseriate epidermis overlying, on the ovule-bearing surface, a 115-mm-thick layer of small (19 mm diam- eter) cells and, on the veined surface, a 365-mm-thick layer of larger (ca 60 100 mm) cells (Fig. 9A–C). Veins were positioned at the gradational boundary between the two mesophyll layers. Ovules were attached on short pedicels over the veins but the vascu- lar strands of the lamina in the available specimens were small and poorly preserved, hence the arrange- Fig. 11. Holotype of Austroglossa walkomii Holmes, 1974 showing ment of xylem and phloem was ambiguous. An oblique the polysperm borne on a long axillary pedicel attached basally to section through one fructification (Gould & Delevoryas the twisted petiole (arrowed) of a glossopterid leaf. In untwisted specimens, the ovuliferous surface faces the subtending leaf. Scale 1977, fig. 5A) intersected a vascular strand consisting bar ¼ 10 mm. of a small, central, cluster of dark cells (?xylem) per- haps surrounded by a cylinder of pale, thin-walled cells Pant & Nautiyal (1984) described the concave, fertile (?phloem), although Nishida et al.(2007) interpreted surface of Ottokaria zeilleri fructifications as adaxial the xylem and phloem to be bifacially differentiated (facing away from the attached leaf). However, it is with the xylem positioned towards the ovuliferous side likely that their fructification illustrated in attachment to of the veins. a leaf has a twisted pedicel. Similarly, Holmes (1974) All other permineralized ovuliferous organs studied illustrated the holotype of Austroglossa walkomii with to date have been isolated from leaves. However, the the fertile surface of the fructification facing away from vascular architecture of these permineralized ovulifer- the subtending leaf. However, the petiole of the subtend- ous organs has been used to interpret their orientation. ing leaf linked to the long pedicel of this organ is clearly Taylor & Taylor (1992), Nishida et al.(2007) and arched and twisted (Fig. 11), and additional attached Ryberg (2010), investigating permineralized fructifica- specimens illustrated in a later study (Holmes 1990) tions from Antarctica and Australia, argued that the reveal the ovuliferous surface to face the leaf. The prob- ovules were borne on the adaxial surface (based on the ability of distortion and twisting of the slender pedicel assumed adaxial position of the xylem within the vas- in laterally compressed specimens (which are by far the cular bundles of the polysperm) entirely by analogy minority of known dictyopteridioid fertiligers) is high. with the vasculature of leaves, and not on the basis of The overwhelming majority of specimens preserved as demonstrated organic attachment between a fructifica- impressions (when correctly interpreted as moulds rather tion and leaf. Taylor & Taylor (1992) also suggested than casts) clearly demonstrate that the seed-bearing sur- that the ovuliferous surface faced away from the leaf face faces the subtending leaf. based, in part, on the proposition that pollination would Permineralized fructifications studied in serial sec- be difficult if the seeds were positioned between the tion from the Homevale locality in Australia appear to fructification lamina and the subtending leaf. However, confirm that the enrolled ovule-bearing surface of the close inspection of the specimens on which these argu- polysperm faces the subtending leaf (Nishida et al. ments are based (Taylor & Taylor 1992, figs 1, 3, Pigg 2018). Despite noting this arrangement, Nishida et al. & Trivett 1994, fig. 31, and Nishida et al. 2007, fig. (2018) interpreted the polysperm’s ovuliferous surface 2a, g, h, Ryberg 2010, fig. 2a, c; Fig. 9A–E) shows ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 499

Adnate Fig. 12 (Continued) Axillary shoot megasporophyll Taylor & Taylor (1992) and Nishida et al.(2007). B, The fertile pinnule model (sensu Ophioglossales) favoured by Kato (1990). C, The shoot-borne megasporophyll model of Doyle (2006). D, The cladode model sensu Florin (1951, 1954) favoured by Schopf (1976) and this study. E, Comparison with the basic architecture of a conifer ovuliferous/bract-scale complex from a composite conifer cone. Red fill indicates a shoot homologue; orange fill indicates a Leaf fertile leaf (megasporophyll) homologue; green fill indicates the subtending sterile leaf/bract.

diminutive xylem packages surrounded on all sides by (A) void space and/or degraded thin-walled cells that might Fertile pinnule sensu represent either parenchyma or phloem. Moreover, the Axillary Ophioglossaceae receptacles of Homevaleia and Lakkosia are enrolled shoot such that the ovules (some of which contain pollen in the micropyles) are covered by the marginal wings, which would provide no less of a barrier to pollination than if positioned between the receptacle and the sub- Leaf tending leaf. Further, the orientation of the ovules should not have hindered pollination as both erect and pendant ovules occur on the ovuliferous scales of dif- (B) ferent extant species of Picea (Owens et al. 1998) and Megasporophyll attached are successfully pollinated. Whether the xylem was adaxial within the strand or situated centrally and sur- Adnate to axillary shoot rounded by a cylinder of phloem in the fertile organs axillary of glossopterids remains equivocal on the basis of cur- shoot rently available anatomical data. Significantly, if (1) the vasculature has been inter- preted correctly in previous studies of permineralized Leaf specimens, and (2) the polysperms are homologous to megasporophylls, then the ovuliferous surface of the polysperm would be structurally adaxial (Fig. 10A). (C) Taylor & Taylor (1992) and Pigg & Trivett (1994) Fertile cladode used this as an argument to infer that the ovuliferous (axillary shoot) surface of the polysperm must have faced away from the subtending leaf. However, this interpretation con- trasts with multiple studies modelling the architecture of impression fossils that have shown consistently that the ovuliferous surfaces of polysperms face towards the Leaf subtending leaf (McLoughlin 1990b, Adendorff et al. 2002, Adendorff 2005, Prevec et al. 2008, Prevec 2011, 2014; Fig. 8). Clarifying the vasculature of the permineralized organs is a high priority for future stud- (D) ies and should resolve whether these fertile organs are Ovuliferous scale homologous with megasporophylls or flattened axillary (fertile axillary shoot) shoots (cladodes). If the fructifications are considered to be the latter, ‘cladosperms’ as suggested by Schopf (1976) and Meyen (1987), then the orientation of the xylem and other tissues is a moot point. Cladodes have been demonstrated to show a broad range of anatomical themes, as outlined below.

Structural relationship of the polysperm to the Bract scale subtending leaf (E) Glossopterids are unique among gymnosperms in pos- Fig. 12. Various models proposed to interpret the homologies of sessing a laminar ovule-bearing organ (polysperm) glossopterid fertiligers. A, The megasporophyll model favoured by emerging from the midrib (or in some cases from the 500 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA axil) of an otherwise normal leaf. Resolving the homol- groups, it is more likely that the superficial similarities ogies of the polysperm among other gymnosperms and between the organs of glossopterids and ophioglossids, how this arrangement of organs originated is key to and also the fruit–cladode or fruit–bract complexes of understanding the phylogenetic relationships of glos- Ruscus (Hirsch 1977) and Tilia (Pigott 2012) are cases sopterids to other plant groups. Constructing a mean- of parallelism. ingful matrix of character states for glossopterids has Schopf (1976) strongly argued that the polysperms been hindered by uncertainties as to whether the fertile were borne on axillary stalks that were typically adnate organs represent true modified leaves (megasporo- to the proximal portion of the leaf. He advanced a phylls; Fig. 12A), an adaxial fertile segment of a leaf hypothesis that the putative early glossopterid fructifi- equivalent to the organization of Ophioglossales (Fig. cation Arberia might represent a simplified axillary fer- 12B), some condensed form of axillary branch system tile branched shoot system homologous to the fertile (perhaps equivalent to the fertile spike of cordaitaleans spikes of cordaitaleans, having achieved its structure or the ovuliferous scale of conifer cones; Fig. 12D, E), through the loss of distichous bracts and the reduction some combination of these structures (Fig. 12C), or of each fertile short shoot of the compound cordaita- something entirely unique. We outline the historical lean cone to a single ovule (Fig. 2A). Scutiform (dic- interpretations of glossopterid relationships and assess tyopteridioid), rigbyoid and lidgettonioid fructifications the probable homologies of glossopterid polysperm-leaf might have, in turn, arisen by reduction and coales- complexes (fertiligers) with a view to refining future cence of the axillary branching system to one or a few phylogenetic analyses. dense ovuliferous receptacles. This hypothesis has Historically, glossopterids were first regarded as some merit but has been challenged on the basis of ferns (Brongniart 1828–38, Feistmantel 1881, 1886). anatomical studies as outlined above (Taylor & Taylor Small tubercles recognized on some of the earliest 1992, Nishida et al. 2007). recorded fructifications (Dictyopteridium) were inter- The architecture envisaged by Schopf (1976)isan preted as sporangia borne on modified leaflets arrangement of organs common in modern and fossil (Feistmantel 1881, 1886). A gymnospermous affinity seed plants (e.g., cordaitaleans, conifers, ginkgoaleans, was demonstrated definitively by Plumstead (1952) dicranophyllaleans; Fig. 12E; Retallack & Dilcher who illustrated seed-bearing organs (polysperms) 1981, Meyen 1987). It is generally called the ‘Florin attached to the midribs of normal Glossopteris leaves. model’ after Rudolf Florin’s extensive work document- Plumstead (1952) interpreted the polysperms to be ing the organization and development of cone systems fertile laminar appendages ‘emerging’ from or in modern and fossil conifers and their relatives. ‘developing on’ the leaf. However, both WN Edwards Florin’s(1951, 1954) hypothesis, which accords with and John Walton, in discussion of Plumstead’s(1952) the ‘polyaxial’ or ‘brachyblast’ theory (that conifer paper, suggested that the fructifications were structur- seed-bearing units represent condensed fertile axillary ally positioned in the axil of the subtending leaf and shoot systems bearing reduced megasporophylls), had that the polysperm pedicel was adnate to the petiole been discussed by botanists throughout the early twen- and lower portion of the leaf lamina. In reply to discus- tieth century (see summary by Coulter & Chamberlain sions of her 1952 article, Plumstead agreed with the 1917, p. 245). Such an arrangement in glossopterids axillary position and adnate character of the polysperm would be expected to yield a vascular organization of pedicel and she incorporated these features in descrip- the fructification more similar to an axis or cladode tions of the South African glossopterid fructifications than to the bifacial vasculature of a typical leaf. In con- in her subsequent (1956a) paper. trast, permineralized glossopterid fructifications, ini- Despite convincing illustrations of the axillary inser- tially illustrated by Gould & Delevoryas (1977) tion of some fructifications (e.g., Austroglossa walko- revealed a laminar form, essentially similar in anatomy mii of Holmes, 1974; Fig. 11), Melville (1983b, to glossopterid leaves (Pigg 1990, Pigg & McLoughlin p. 282) stated that ‘there is no evidence that the fertile 1997). As outlined above, if the polysperms were branch of Glossopteridae was ever axillary’. He sug- indeed homologous to leaves, and if their vasculature gested that the fertile organs were epiphyllous has been interpreted correctly in studies of the permin- branches. This notion has received little support from eralized specimens (with xylem adaxial in the strands; later research, although Kato (1990) raised the hypoth- Taylor & Taylor 1992, Pigg & Trivett 1994, Nishida esis that the glossopterid polysperm represented an et al. 2007, Ryberg 2010), then the ovuliferous surface adaxial fertile segment (¼sporophore) of the subtending of the fructification would be adaxial. Because glossop- leaf (¼trophophore) analogous to the fertile appendage terid fertiligers typically consist of a polysperm borne of Ophioglossales (Fig. 12B). He argued (Kato 1990,p. in the axil of, or adnate to the midrib of, a vegetative 310) that, if this were the case, then ‘glossopterids leaf, Taylor & Taylor (1992) recognized that posses- might occupy an intermediate evolutionary position sion of a fertile leaf emerging from the axil of another between ophioglossids and angiosperms’. However, (normal) leaf would represent a structural arrangement owing to their representation in widely disparate not seen in modern seed plants. Nevertheless, they ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 501 suggested that perhaps glossopterids adopted a morpho- logical bauplan (here designated the ‘Taylor model’)no longer represented in modern plants (Fig. 12A). Doyle (2006) presented an additional model (essen- tially equivalent to an architecture presented by Retallack & Dilcher 1981, fig. 3B) that sought to resolve the apparent conflict between the ventral pos- ition of ovules on the polysperm detected in studies of impression fossils and the adaxial position inferred from fructification vascular anatomy. He argued that if the polysperm represented a megasporophyll attached to a dormant axillary shoot/bud that was adnate to, or carried up onto, the subtending leaf midrib during leaf expansion, then the ventral (seed-bearing) surface of the megasporophyll would be structurally adaxial with respect to the dormant axillary shoot (Figs 10B, 12C). Doyle’s(2006) model adds an extra structural compo- nent making the polysperm a two-part organ (adnate axillary axis þ megasporophyll). Given that the inter- pretation of the fructification vasculature remains equivocal, as outlined in the previous section, inference of this additional structure (the megasporophyll) may be unnecessary. Aase (1915), Nakayama et al.(2012) and Yamada & Yamada (2017) have shown that, in at least some conifer and angiosperm groups, ovuliferous scales and cladodes can develop a bifacial, leaf-like anatomy but with inverted vasculature (i.e., having the xylem distributed abaxially and the phloem adaxially in the veins). If the Fig. 13. Schematic reconstruction of the components of an xylem were positioned abaxially in glossopterid poly- ovuliferous glossopterid loose strobilus based on shoots with attached sperms, consistent with the orientation of the ovules from Lidgettonia fertiligers presented by Prevec & Matiwane (2018). impression fossils (McLoughlin 1990a, 1990b,Prevec et al. 2008,Prevec2011, 2014), then these structures can Matiwane 2018). The loose arrangement of fertiligers be interpreted as fertile axillary cladodes essentially hom- to form a lax compound cone (Fig. 13), together with ologous with the ovuliferous scales of conifers (Figs 10C, the production of simple pollen-bearing cones (White D, E, 12E). This arrangement provides a model that is 1978), represent additional similarities to conifers but, consistent with both the anatomical and morphological because the organization of the reproductive organs is evidence and negates the need to invoke an additional not known for many derived (Mesozoic) seed-fern structure—the megasporophyll of Doyle (2006). groups, it is uncertain how diagnostic this character is Few studies have provided unequivocal evidence for segregating clades of extinct seed plants. concerning the arrangement of the fertiligers on the parent plant (i.e., whether they were borne in isolation Towards a consensus on fructification architecture or were aggregated in some way on the host branch). Several authors have noted examples of dictyopteridi- Here we summarize our interpretation of the architec- oid fructifications in close aggregations, athough not tures of the four families most commonly recognized directly attached to a parent axis (Holmes 1974, Pant among glossopterids. These structural interpretations & Nautiyal 1984, Anderson & Anderson 1985, will form the basis of a future systematic revision of McLoughlin 1990c) suggesting some degree of cluster- the constituent genera established for glossopterid ovu- ing of the reproductive units. Lacey et al.(1975) and liferous fructifications. White (1978) suggested, albeit based on little support- Although superficially megasporophyll-like in ing data, that some lidgettonioid fertiligers were borne morphology, an axillary position and cladode-like anat- in lax cones. This inference has recently been borne omy seems to be the most parsimonious interpretation out in two studies, one of a permineralized immature of glossopterid polysperms. Their apparent emergence cone-like structure from Australia attributable to either from the midrib of a glossopterid leaf appears to be the Lidgettoniaceae or Dictyopteridiaceae (Nishida et al. result of an axillary fertile branch being partly fused to 2018), and a second of impression fossils the subtending leaf midrib. Confirmation of this (Lidgettoniaceae) from South Africa (Prevec & hypothesis will ultimately require serial sectioning or 502 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA tomographic reconstructions of three-dimensional, ana- tomically preserved, leaf-fructification complexes.

Dictyopteridiaceae. The landmark paper of Gould & Delevoryas (1977) describing the anatomical struc- ture of Dictyopteridium-like polysperms preserved as siliceous permineralizations confirmed that these organs were flattened, bifacial, at least superficially leaf- or bract-like structures bearing ovules on one surface. The lateral wings represented narrow extensions of the receptacle that were folded over the ovuliferous sur- face, at least during the early stages of development (Gould & Delevoryas 1977, Nishida et al. 2018), but there was no separate protective bract. Once anatomically preserved specimens were described, adpression fossils were generally reinter- preted according to the architecture outlined by Gould & Delevoryas (1977). Among these later studies of adpression fossils were key reviews and descriptions of new taxa by Banerjee (1984), Pant & Nautiyal (1984), Anderson & Anderson (1985), Holmes (1990), Maheshwari (1990), McLoughlin (1990a, 1990b, 1995, 2012a, 2012b, 2012c, 2016), Adendorff et al. (2002), Adendorff (2005), Prevec (2011, 2014), Prevec et al. (2008), Cariglino et al.(2009), Ryberg (2009), Cariglino (2013, 2015), Ryberg & Taylor (2013), Tiwari & Chauhan (2013) and Marques-de-Souza & Iannuzzi (2016). Many of the polysperms, previously interpreted as cone-like, were easily reinterpreted as flattened or enrolled laminar structures. Our reinterpretation of scutiform (¼dictyopteridioid) glossopterid fructifications (Figs 10C, 12D) provides a means of unifying the contradictory interpretations derived from permineralized and impression fossils. The polysperms can now be interpreted as condensed axillary branch systems (fertile cladodes partially adnate to the subtending leaf) with abaxially positioned xylem and abaxial ovules facing the leaf (Figs 12D, 13, 14A), and not megasporophylls. Thus, we consider glossopterid fertiligers to be consistent with the Florin model. The polysperms attached to a subtending leaf (collectively forming fertiligers) in glossopterids (Fig. 14A–D) would be homologous to the variably free or fused ovuliferous-/bract-scale complexes of conifers (Figs 10C–E, 12E, 15) that were derived from a more lax cone of a Cordaites-like ancestor. The stratigraphic distribution of character states provided by the fossil Fig. 14. Stylized reconstructions of the fertiligers of the four record of both glossopterid and cordaitalean-conifer lin- established families of glossopterids. A, Dictyopteridiaceae (with eages suggests that there has been independent evolu- scutiform polysperms). B, Lidgettoniaceae (with multiple cupule-like tion of common traits long after the differentiation of fertile units). C, Rigbyaceae (with flabellate polysperms and inferred axillary insertion). D, Arberiaceae (with branched polysperms and these clades. This has generally involved reduction of inferred axillary insertion). the fertile axillary shoot and the number of ovules, planation of the shoot to form a leaf- or scale-like clad- ode, and variable recurvature, enclosure or embedding of glossopterids remained much less condensed than of the ovules in the cladode for protection from desic- the compact cones of conifers, (2) the subtending bracts cation or herbivory (Fig. 15). The only substantial dif- remained more leaf-like in glossopterids (with the ferences between these lineages being: (1) the strobili exception of Lidgettoniaceae) and became scale-like in ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 503

CORDAITALES & PINALESGENERAL GLOSSOPTERIDALES (DICTYOPTERIDIALES) EVOLUTIONARY OS P Lidgettonia TRENDS mucronata

SBr Progressive enclosure/ protection of ovules Pinus sp. BS Reduction of subtending bract P SBr Dictyopteridium OS sporiferum

Adaxial (in conifers) and P abaxial (in glossopterids) recurvature of ovules Glyptolepis BS on polysperm longibracteata Rigbya arberioides SBr

OS Planation of fertile axillary shoot, P loss or fusion of associated bracts

BS

Ernestiodendron filiciforme Arberia madagascariensis SBr Br P

P

Krylovia/Rufloria SBr SBr Reduction of bracts & megasporophylls Lebachia lockardii Condensation of fertile axillary shoot

Arberia minasica SBr A Br

Ms

Ancestral state represented by loose strobili of fertile axillary short shoots bearing spirally arranged megasporophylls and scales, SBr collectively borne in the axils of larger subtending bracts Cordaitanthus conncinus

Fig. 15. Schematic diagram showing hypothesized parallel evolutionary patterns of condensation and planation of axillary ovule-bearing organs of cordaitaleans, conifers and glossopterids. A ¼ axis, Br ¼ bract, BS ¼ bract scale, Ms ¼ megasporophylls, OS ¼ ovuliferous scale, P ¼ polysperm (cladode), SBr ¼ subtending bract. 504 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA conifers, and (3) the ovules in conifers are borne on architectural interpretation. They are flattened, flabel- the adaxial surface (or on adaxially recurved lobes) of late, bilaterally symmetrical organs with a pedicel ter- the ovuliferous scale, whereas in glossopterids, the minating in pairs of dichotomous branches that may be ovules are borne on the abaxial surface and the recep- fused to varying degrees into a fan-shaped receptacle, tacle is commonly folded longitudinally for protection or may dichotomize several times to form a fan of free during early development. In other words, the plesio- terminal branches. A single seed is borne on each ter- morphic condition of the ovuliferous ‘scale’ of conifers minal lobe or branch, and is flanked distally by a stri- and the polysperm of glossopterids probably was radial ate flange homologous to a single segment of the wing symmetry, and it was through planation and loss of of scutiform fructifications (Figs 1I, J, 2B, 5P, Q, branches on contrasting surfaces of the shoot that 14C). The wing/flange segments may be equivalent to resulted in the conifer (adaxial) versus glossopterid reduced megasporophylls in an evolutionary sense, (abaxial) distribution of seeds. since early conifers and cordaitaleans bear possibly homologous reduced seed-bearing scales (¼leaves) on Lidgettoniaceae. Less controversy has surrounded their fertile axillary shoots (Rothwell 1982, Mapes & the morphological interpretation of fructifications, such Rothwell 1991). as Lidgettonia, which consist of several receptacles The only exception to this standard interpretation attached by pedicels to the medio-longitudinal portion was invoked by Melville (1983a, 1983b), who consid- of a single (generally very reduced) glossopterid leaf ered Mudgea (¼Rigbya) fructifications to possess two (Figs 1N, 2C, 14B). Most researchers have considered sets of terminal scales—lanceolate sterile or microspor- the individual receptacles of this group to represent angiate scales alternating between obovate seed-bearing discs or cupules with varying degrees of enclosure of scales along the distal rim of the receptacle. Melville the seeds (Thomas 1958), each cupule (Figs 13B, 14B) (1983b) favoured the interpretation of these organs as being structurally equivalent to a reduced polysperm of bisexual, drawing homologies with ranunculacean flow- Dictyopteridiaceae (Fig. 14A). The only differing views ers. However, the lanceolate scales reported by were those of Surange & Maheshwari (1970) and Melville represent creases located between the bases of Surange & Chandra (1973c) who considered the fructi- the fertile lobes on the expanded receptacle and do not fications of Lidgettonia indica to consist of either a bear pollen. The thin strips of tissue around the ovules cluster of four seeds or four separate seed-bearing in the superficially ‘cupulate’ form of Lakkosia kera- cupules at the end of each pedicel. Forms attributed to sata from Antarctica (Zhao et al. 1995, Taylor et al. Lidgettonia (the senior synonym of Partha, Rusangea 2007, Ryberg 2010) may represent oblique sections and Mooia) represent relatively open cupules, or even through the terminal scales/flanges that form a distal reduced spathulate structures typically bearing several fringe around rigbyoid polysperms. Schopf (1976) illus- seeds on the surface facing the attached leaf (Figs 1M, trated impressions of Rigbya polysperms from the same N, 5M, N). Denkania was interpreted to produce more region of Antarctica with similar arched flanges adja- enclosed cupules possibly bearing a single seed cent to the seeds. (Surange & Chandra 1973b, 1975), although our obser- Rigbya and Nogoa fructifications have never been vations suggest at least two seed scars were present per found attached to leaves, although their co-preservation cupule in this genus (Fig. 5O). The reproductive archi- with broad-meshed forms of Glossopteris strongly tecture of this family is consistent with that of favours a biological association (Anderson & Anderson Dictyopteridiaceae except that the fertile axillary shoot 1985, McLoughlin 1994, Prevec 2016). This, together is divided into several polysperms. In this respect, lidg- with their generally long pedicel, suggests that they ettonioid fructifications somewhat parallel the architec- were borne in the axil and dispersed in isolation from ture of some early conifers, such as Ernestiodendron the subtending leaf. Nevertheless, they appear to con- filiciforme (Fig. 15), in which the ‘ovuliferous scales’ form to the glossopterid bauplan in that the polysperms consist of several discrete ovule-bearing units fused at represent bifacial, multiovulate, axillary cladodes their bases (Florin 1944). Lidgettoniaceae polysperms (Fig. 14C). also differ from those of Dictyopteridiaceae in being small and, in some cases, having strongly arched wings Arberiaceae. The fourth group of putative glossop- that partially enclose the seeds to produce a cupular terid ovuliferous organs, exemplified by Arberia (Figs morphology. Similar to the condition in 1K, L, 2A), was interpreted by Schopf (1976)tobea Dictyopteridiaceae, the divided axillary shoot is adnate fertile axillary branch system bearing irregularly dis- to the proximal part of a leaf, which in Lidgettoniaceae tichous ovuliferous appendages representing simplified is somewhat reduced to a scale-like, or otherwise modi- homologues of the distichous fertile short shoots of fied, subtending bract (Fig. 14B). cordaitalean cones. Following Millan (1967), Schopf (1967) suggested that Arberia might be affiliated with Rigbyaceae. Rigbyoid glossopterid fructifications Noeggerathiopsis but that scutiform fructifications were have, similarly, attracted little controversy in their structurally similar in that they too were much ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 505 modified, condensed, axillary, fertile shoots partly adnate to a subtending leaf. Surange & Lele (1957) described Arberia umbellata Angiosperms Lyginopteridales Medullosales Cycadales Cordaitales Pinales Ginkgoales Callistophyton Peltaspermales Glossopteridales Caytoniales Umkomasiales Pentoxylales as a megasporophyll-like organ with seeds borne on Bennettitales Gnetales terminal recurved processes. The organs can, alterna- tively, be interpreted as fertile axillary axes with recurved, ovuliferous termini. Chandra & Srivastava (1981) considered several models to interpret the struc- ture of Arberia surangeii fructifications but were unable to conclude whether the fructifications were (A) homologous to megasporophylls or fertile branch com- plexes. Appert (1977) described the fructifications of Dolianitia (¼Arberia) madagascarensis as ‘megastrobili’ but acknowledged that the seed-bearing Angiosperms Ginkgoales Bennettitales Lyginopteridales Medullosales Umkomasiales Cordaitales Pinales Pentoxylales Gnetales Peltaspermales Glossopteridales Caytoniales Cycadales appendages appeared to be positioned laterally and uni- Callistophytales facially on the main body rather than arranged spirally. The same arrangement is apparent in both South American (Rigby 1972a, pl. 24, fig. 5) and Indian (Chandra & Srivastava 1981, pl. 1, figs 1–3) Arberia species, with ovuliferous branches produced both mar- ginally and across only one side of the broad, flattened (B) primary axis. The mid-laminal branches appear to have protruded into the sediment during burial, producing (peltasperm) indentations in the matrix that are apparent only on the + part and not the counterpart of the impression fossil. Angiosperms Ephedra Umkomasiales Lyginopteridales Medullosales Callistophyton Peltaspermum Tartarina Cordaitales Ginkgoales Pinales Pentoxylales Bennettitales Gnetum Welwitschia Cycadales The unifacial production of these mid-laminal branches Glossopteridales Caytoniales and the orientation of the marginal lateral branches with seed scars all positioned on the same side of the bifacial fructification, results in an organ with one entirely veined surface, and the other bearing all of the seed attachments. The bifacial nature of these Cisuralian fructifications lends support to the concept (C) of an increasingly condensed and planated branch com- ‘glossophytes’ plex to describe the origins and homologies of the scu- tiform glossopterid fructifications, provided the arberioids are in fact glossopterid in their affiliations Autunia Angiosperms Pinales Glossopteridales Lyginopteridales Gnetales Bennettitales Callistophyton Ginkgoales Caytoniales Pentoxylales (Fig. 15). Medullosales Cycadales Peltaspermum Umkomasiales Cordaitales As yet, arberioid fructifications have not been found attached to foliage so attribution to the glossopterids can not be confirmed. Nevertheless, the striate flange- like structures flanking the seed attachment points on some Arberia specimens (Figs 1L, 5S) are morpho- logically similar to, and probably homologous with, the ‘glossophytes’ (D) ‘higher marginal wing segments of confirmed glossopterid seed-ferns’ fructifications, and are particularly congruous with those of Rigbya and Nogoa (Figs 1I, J, 5P, Q). Given their consistent isolation from foliage, we infer that Autunia Angiosperms Pinales Gnetales Glossopteridales Caytoniales Callistophyton Umkomasiales Pentoxylales Lyginopteridales Medullosales Cycadales Peltaspermum Arberia polysperms were borne in an axillary position Ginkgoales Cordaitales Bennettitales (Figs 14D, 15).

Implications for phylogenetic placement of glossop- terids. Several authors have undertaken major phylo- genetic analyses over the past four decades incorporating a broad range of fossil seed-plant groups (E) including glossopterids (Crane 1985, Doyle & Donoghue 1992, Nixon et al. 1994, Rothwell & Serbet Fig. 16. Simplified results from key phylogenetic analyses of major 1994, Doyle 2006, Hilton & Bateman 2006). extant and fossil seed plants, colour coded to highlight equivalent 506 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

Fig. 16 (Continued) closer affiliations with conifers and cordaitaleans than plant groups. Cladograms differ in their topology with respect to recovered in most previous analyses. In the absence of glossopterids (green) depending principally on the coding of fundamental data for the reproductive characters of characters for seed and ovuliferous fructification architecture. A, Crane’s(1985, fig. 20) strict consensus tree derived from five many fossil plant groups, a revised phylogenetic ana- equally parsimonious cladograms constructed from a version of the lysis of seed plants is premature. In particular, detailed data matrix in which the ‘cupules’ of Bennettitales and Pentoxylon re-analyses of the reproductive organs of Mesozoic ‘ ’ were not coded as homologous to the cupules/polysperms of seed-ferns are required to assess their structural homol- glossopterids, Caytonia, corystosperms and angiosperms; glossopterids are nested within a broad clade of conifers, ogies in order to obtain any meaningful results from a cordaitaleans, ginkgoaleans and Mesozoic seed-ferns. B, Strict future phylogenetic analysis of seed plants. consensus tree of most parsimonious trees resulting from an analysis in which all characters except one were assumed to be reversible and multistate characters were assumed to be unordered (from Rothwell & Serbet 1994, fig. 4a); glossopterids are nested in a relatively basal Conclusions and future prospects clade of Mesozoic seed-ferns. C, Strict consensus tree of Nixon et al. Over 40 genera of fructifications have been established (1994, fig. 10) derived from their matrix III, in which glossopterids for ovuliferous glossopterid fructifications with new are positioned basal to the peltasperm Tartarina, conifers, cordaitaleans, ginkgoaleans, bennettitalens, pentoxylaleans, gnetaleans taxa being circumscribed regularly. Six genera have and angiosperms. D and E strict consensus trees from (D) Doyle been established in the past decade based on both per- (2006, fig. 6) of eight most parsimonious trees obtained from an mineralized and adpression material and it seems likely unconstrained analysis, and (E) Hilton & Bateman (2006, fig. 4) of 21 most parsimonious trees, each showing glossopterids in different that additional diversity will be recognized within this topological positions within a broad ‘glossophyte’ clade group as new fossil assemblages are described. encompassing most Mesozoic seed-ferns, bennettitaleans, However, we note that many of the established genera pentoxylaleans, gnetaleans and angiosperms. are synonyms, being founded on erroneous interpreta- tions of polysperm morphology under different states Characters of the ovuliferous organs play a key role in of preservation. Further, some taxa are invalid owing to influencing the topology of the resulting phylogenetic nomenclatural conflicts with the rules of the ICN trees. Several of the most parsimonious trees place (Turland et al. 2018), and others may even represent glossopterids in key positions at the base of the misinterpretations of arthropod galls or oviposition ‘ ’ ‘ ’ anthophyte or glossophyte clade in various relation- damage (Bordy & Prevec 2008, McLoughlin 2011a). A ships with Mesozoic seed-ferns, Bennettitales, thorough revision of glossopterid reproductive organ – Pentoxylales, Gnetales and angiosperms (Fig. 16A E). taxonomy is necessary to resolve the diversity within However, our evaluation of the features of the ovulifer- the group. Such a review is likely to reduce the number ous organs used in these analyses (Online supplemen- of existing genera owing to widespread synonymies, tary Table 1), combined with a reassessment of ovule/ but will also require the establishment of some new seed characters by McLoughlin et al.(2018, table 9.2) taxa to accommodate certain species with morphologies suggests that many of the characters used in the matri- that do not fall comfortably within the existing gen- ces of these earlier studies have been scored incor- eric spectra. rectly. In particular, future phylogenetic analyses will A taxonomic revision of genera encompassing glos- need to: sopterid fructifications and an improved understanding 1. Score glossopterid fertiligers as being aggregated of linkages between taxa established for different fossil into loose compound strobili. organs is also essential before any meaningful phylo- 2. Score glossopterid polysperms as axillary fertile genetic analysis can be undertaken within the order. shoots (cladodes) rather than strictly Identification of linkages between organs will provide megasporophylls. improved whole-plant concepts for glossopterid species 3. Recognize the diversity of architectural styles and facilitate a better understanding of the range of within glossopterids including, among other ecological strategies within the order. Moreover, some features, both branched and unbranched bifacial glossopterid genera appear to have narrow geographic polysperms, variable placement of ovules between distributions and short ranges within the Permian and the margins and flattened face of the polysperms, are potentially useful as biogeographic and biostrati- and recurved ovuliferous branchlets and cupule-like graphic indices within continental strata (McLoughlin structures in some taxa. 1993, 2001, Bordy & Prevec 2008, Shi et al. 2010). 4. Score the insertion of the ovules on the polysperms Additionally, the fructifications have morphologies that as abaxial. are more diagnostic for glossopterids than the leaves, 5. Recognize longitudinal folding of the ovule-bearing which have few unique characters. Homoplasy may structure in glossopterids in contrast to transverse have resulted in the development of similar leaves in folding in some Mesozoic seed-ferns. other gymnosperms, hence the stratigraphic distribu- Reinterpretation of glossopterid ovuliferous organs tions of the fructifications are crucial for testing the to conform to the Florin model is likely to favour veracity of putative holdover (relictual) occurrences of ALCHERINGA PERMIAN GLOSSOPTERID OVULIFEROUS REPRODUCTIVE ORGANS 507 glossopterids beyond the end-Permian extinction event Funding (Bomfleur et al. 2018, Fielding et al. 2019). Financial support from the following organizations is Our re-evaluation of the morphology and anatomy gratefully acknowledged: to SM—Swedish Research of glossopterid fertiligers provides an architectural Council [VR grants 2014-5234, 2018-04527] and model that is consistent with evidence from both National Science Foundation [project #1636625]; to adpression and permineralized fossils. Moreover, our RP—University of the Witwatersrand, Rhodes favoured architecture, interpreting the glossopterid pol- University, the DST-NRF Centre of Excellence in ysperm as a flattened fertile cladode emerging from the Palaeosciences and the NRF African Origins Platform axil of a glossopterid leaf, is largely consistent with the [UID: 98822]. model espoused for cordaitaleans and conifers by Florin (1951, 1954) and for various other late Palaeozoic seed plants by Meyen (1987). Improved Supplemental data resolution of the glossopterid polysperm architecture Supplemental data for this article can be accessed here. and its relationship to the subtending leaf will be needed to ultimately confirm the ‘Florin model’ for glossopterid fertiligers. Non-destructive analysis via References X-ray or neutron tomography of permineralized speci- AASE, H.C., 1915. Vascular anatomy of the megasporophylls of coni- fers. Botanical Gazette 60, 277–313. mens potentially offers the best opportunities for ADENDORFF, R., 2005. A Revision of the Ovuliferous Fructifications of resolving this issue. Glossopterids from the Permian of South Africa. PhD thesis, The arrangement of glossopterid fertiligers in loose University of the Witwatersrand, Johannesburg, 422 pp, 100 pls. compound strobili provides further evidence of shared (unpublished) ADENDORFF, R., MCLOUGHLIN,S.&BAMFORD, M.K., 2002. A new characters with conifers and cordaitaleans. On this genus of ovuliferous glossopterid fruits from South Africa. basis, we suspect that once these characters and other Palaeontologia africana 38,1–17. features of the seeds, microsporophylls and vegetative ANDERSON, J.M. & ANDERSON, H.M., 1985. Palaeoflora of Southern anatomy are revised within character matrices (see, Africa. Prodromus of South African Megafloras Devonian to Lower Cretaceous. A.A. Balkema, Rotterdam, 416 pp. e.g., McLoughlin et al. 2018 for erroneous character ANDERSON, J.M., ANDERSON, H.M. & CLEAL, C.J., 2007. Brief History states interpreted previously for seeds), glossopterid of the Gymnosperms: Classification, Biodiversity, relationships within general phylogenies of seed plants Phytogeography and Ecology. Strelitzia 20. South African may alter significantly to reveal closer affiliations to National Biodiversity Institute, Pretoria, 280 pp. APPERT, O., 1977. Die glossopterisflora der Sakoa in sudwest-€ conifers, cordaitaleans and ginkgoaleans, rather than Madagaskar. Palaeontographica 162B,1–50. the traditional view that they belong in the poorly ARBER, E.A.N., 1905. On the sporangium-like organs of Glossopteris defined and almost certainly paraphyletic ‘seed-ferns’ browniana. Quarterly Journal of the Geological Society 61, – (pteridosperms). We await further re-evaluation of 324 338. BANERJEE, M., 1968.OnScutum stowanum Plumstead, the fructifica- microsporangiate and vegetative characters of glossop- tion borne by Glossopteris decipiens Feistm. from the Raniganj terids before undertaking a phylogenetic analysis of Stage of India and cuticular study of the fertile and vegetative this group and of seed plants as a whole. leaves of G. decipiens Feistm. Bulletin of the Botanical Society of Bengal 22, 165–168. BANERJEE, M., 1973. Glossopteridean fructifications: 1. Dictyopteridium sporiferum Feistmantel. Bulletin of the Botanical Acknowledgements Society of Bengal 27,77–84. Some of the material presented here contributed BANERJEE, M., 1978. Glossopteridean fructifications: 2. On the revi- towards the PhD degree of RP at the University of the sion of Ottokaria Zeiller and the occurrence of O. raniganjensis Witwatersrand (Adendorff 2005). We thank the cura- Banerjee from the Raniganj Formation (Upper Permian) of India. Indian Journal of Earth Sciences 5, 129–140. tors and collection managers of the many institutions BANERJEE, M., 1984. Fertile organs of the Glossopteris flora and their hosting glossopterid fossils that assisted us in locating possible relationship in the line of evolution. In Proceedings of a and photographing relevant specimens. We thank Symposium on Evolutionary Botany and Biostratigraphy. A.K. Pollyanna von Knorring for preparing the reconstruc- Ghosh Commemoration Volume.SHARMA, A.K., ed., Today and Tomorrows Printers and Publishers, New Delhi, 29–59. tion of glossopterid fertiligers in Fig. 14. We thank BENECKE, A.K., 1976. Several new forms of Glossopteris fructifica- three reviewers and the assistant editor (Chris Mays) tions from the Beaufort Daptocephalus-Zone (Upper Permian) of for their constructive critiques of the manuscript. Natal, South Africa. Palaeontologia africana 19,97–125. Finally, we thank the Chief Editor for his invitation to BOMFLEUR, B., BLOMENKEMPER, P., KERP,H.&MCLOUGHLIN, S., 2018. Polar regions of the Mesozoic–Paleogene greenhouse world as prepare this paper as a contribution to the Nelly refugia for relict plant groups. In Transformative Paleobotany: Ludbrook review series. Papers to Commemorate the Life and Legacy of Thomas N. Taylor.KRINGS, M., HARPER, C.J., CuNEO, N.R., ROTHWELL, G.W., eds, Elsevier, Amsterdam, 593–611. Disclosure statement BORDY, E.M. & PREVEC, R., 2008. Sedimentology, palaeontology and palaeo-environments of the Middle (?) to Upper Permian No potential conflict of interest was reported by Emakwezini Formation (Karoo Supergroup, South Africa). South the authors. African Journal of Geology 111, 429–458. 508 STEPHEN MCLOUGHLIN and ROSE PREVEC ALCHERINGA

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