Reconstruction of a bennettitalean flower from the Carnian (Upper Triassic) of Lunz, Lower Austria

Review of Palaeobotany and Palynology 159 (2010) 94–111

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Reconstruction of a bennettitalean flower from the Carnian (Upper Triassic) of Lunz, Lower Austria Christian Pott a,⁎, Michael Krings b, Hans Kerp c, Else Marie Friis a a b c

Naturhistoriska riksmuseet, Sektionen för paleobotanik, Box 50007, 104 05 Stockholm, Sweden Bayerische Staatssammlung für Paläontologie und Geologie und GeoBio-CenterLMU, Richard-Wagner-Straße 10, 80333 Munich, Germany Institut für Geologie und Paläontologie, Westfälische Wilhelms-Universität Münster, Hindenburgplatz 57, 48143 Münster, Germany

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Article history: Received 18 March 2009 Received in revised form 1 October 2009 Accepted 7 November 2009 Available online 17 November 2009 Keywords: Bennetticarpus Bennettitales cuticular analysis Cycadolepis Haitingeria reproductive biology Upper Triassic Nilssoniopteris

a b s t r a c t The Bennettitales are a Mesozoic group of gymnosperms with complex reproductive organs that figure prominently in hypotheses on the ancestry and origin of angiosperms. However, the exact phylogenetic position of the Bennettitales is still debated, due in part to the scarcity of conclusive fertile remains from the Triassic. In this study we reconstruct a bennettitalean flower from isolated parts from the Carnian (Upper Triassic) of Lunz in Lower Austria, including Cycadolepis wettsteinii scale leaves, Haitingeria krasseri pollen organs, and Bennetticarpus wettsteinii ovulate organs/seed cones, based on correspondences in gross morphology and epidermal anatomy. The flower has small pollen organs with spreading and well-exposed pollen sacs; pollen sacs are not organised in synangia, and the ovulate organ is characterised by a low number of relatively large seeds and a large number of interseminal scales in relation to ovules/seeds. The flower lacks several of the characteristic features seen in geologically younger bennettitaleans, including fused, inwardly curved pollen organs and large number of small seeds. The association of these isolated organs to a single flower provides a rare opportunity to assess the attribution of these early representative of the Bennettitales, and sheds new light on the evolutionary history and phylogenetic position of this ancient group of seed plants. © 2009 Elsevier B.V. All rights reserved.

1. Introduction The Bennettitales are an extinct lineage of Mesozoic (Late Triassic– Late Cretaceous) seed plants characterised by cycad-like foliage and flower-like reproductive organs (e.g., Crane, 1988; Cleal, 1993; Taylor et al., 2009: p. 722). The group has received considerable attention as a possible sister to the angiosperms (e.g., Sharma, 1976, 1977; Bose et al., 1984; Crane, 1985; Watson and Sincock, 1992; Nixon et al., 1994; Donoghue and Doyle, 2000; Rothwell and Stockey, 2002; Stockey and Rothwell, 2003; Hilton and Bateman, 2006; Friis et al., 2007), and in some phylogenetic analyses it is nested with the Gnetales and angiosperms in the so-called anthophyte clade (Crane, 1988; Doyle, 1996; Hilton and Bateman, 2006; Friis et al., 2007). The anthophyte concept is, however, not universally accepted (e.g., Mathews, 2009; Rothwell et al., 2009) and there is currently no consensus regarding the interrelationships among the various groups of extant and extinct seed plants (Nixon et al., 1994; Rothwell and Serbet, 1994; Doyle, 2006). Resolving the phylogeny of seed plants and establishing the exact position of the Bennettitales remains difficult, due in part to the inherent uncertainties regarding the

⁎ Corresponding author. E-mail address: [email protected] (C. Pott). 0034-6667/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.revpalbo.2009.11.004

interpretation of the various bennettitalean reproductive organs and how these should be compared with the ovulate and sporangiate organs produced by other seed plants (e.g., Friis et al., 2009; Rothwell et al., 2009). Moreover, the earliest stages in the evolution of the Bennettitales remain largely elusive because the fossil record of reproductive structures from the Triassic is strikingly sparse (Crane, 1988). In contrast to the Jurassic and Cretaceous record, which includes numerous articulated bennettitalean reproductive organs known from permineralisations and compression fossils (Nathorst, 1888, 1902; Lignier, 1903; Nathorst, 1909; Wieland, 1909; Nathorst, 1911; Schuster, 1911; Wieland, 1916; Sahni, 1932; Harris, 1944; Bose, 1968; Harris, 1969; Crepet, 1974; Sharma, 1976, 1979, 1980; Bose et al., 1984; Crane, 1985; Delevoryas, 1991; Watson and Sincock, 1992; Stockey and Rothwell, 2003; Schweitzer and Kirchner, 2003; Cantrill and Hunter, 2005), the Triassic record primarily consists of isolated flower parts and fragmentarily preserved organs (Krasser, 1912, 1917, 1919a,b; Harris, 1932; Kräusel, 1948, 1949; Kräusel and Schaarschmidt, 1966; Ash, 1968; Pedersen et al., 1989; Ash and Litwin, 1996; Anderson and Anderson, 2003; Anderson et al., 2007). This paper presents a reconstruction of an early bennettitalean flower from the Carnian (Upper Triassic) of Lunz in Lower Austria based on isolated compressions of different flower parts, including scale leaves of Cycadolepis wettsteinii Kräusel, pollen organs of Haitingeria krasseri (Schuster) Krasser, and ovulate organs/seed cones of

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Fig. 1. Map of the region of Lunz-am-See in Lower Austria, showing the locations where Lunz plants have been discovered.

Bennetticarpus wettsteinii (Krasser) Kräusel. The fossils are interpreted as parts of the same flower based on correspondences in gross morphological features (e.g., size, shape of the foliar parts, abscission areas) and epidermal anatomy. The flower was probably borne on plants that produced Nilssoniopteris angustior (Stur ex Krasser) Pott et al. sterile foliage; this association is based on similarities in epidermal anatomy. 2. Geological setting, material and methods The specimens were collected in the late 19th and early 20th centuries from several active coal mines around Lunz-am-See in the Northern Calcareous Alps, Lower Austria, approximately 100 km west of Vienna (Fig. 1). The fossils come from the “Lunzer Sandstein”, which is part of the Lunz beds. The Lunz Formation (=Lunzer Schichten) consists of sandstones at the base, followed by marine marls that grade upwards into terrestrial sands, shales, and coal. The coal-bearing part of the sequence is overlain by marls followed by a sandstone layer. The plant fossils occur in the shales associated with the coal beds. Exact dating of the Lunz Formation remains problematic due to the lack of adequate index fossils such as ammonoids and conodonts. A recent regional and facies-spanning correlation of biostratigraphically well-established sections of the Hallstatt and Reifling Intraplatform basins (Hornung and Brandner, 2005) suggests that the Lunz Formation correlates to the upper part of the Reingraben Formation, and thus is probably late Julian (Julian 2/II) in age. Palynological studies indicate a Carnian (Bharadwaj and Singh, 1964) and Julian age (Dunay and Fisher, 1978; Roghi, 2004). The Opponitzer Limestone, the upper sub-unit of the Lunzer Schichten, has been dated as Tuvalian by Dunay and Fisher (1978). The plant fossils from Lunz are usually preserved as compressions, often with excellently preserved cuticles. Cuticles were prepared according to procedures outlined in Kerp (1990) and Kerp and Krings (1999). Rock samples with plant remains were dissolved in hydrofluoric acid (HF) in order to remove the sediment. Cuticles were macerated using Schulze's reagent (35% HNO3 with a few crystals of KClO3), and subsequently treated with a 5–10% potassium hydroxide (KOH) solution. Macerated cuticles were washed in distilled water,

gently dehydrated in pure glycerine, and finally mounted in permanent glycerine-jelly microscope slides. Slides are stored in the collections of the relevant museums; specimen numbers are included in the figure captions. Specimens were photographed with a Nikon D100 digital camera; in order to enhance contrast, cross-polarisation (i.e., polarised light sources together with an analysing filter in front of the camera lens) was used. Cuticles were analysed with a Leitz Diaplan microscope and photographed with a Nikon DS-5M digital camera. The material included in this study is kept in the following collections: Geological Survey of Austria, Vienna, Austria (GBA), Museum of Natural History, Vienna, Austria (NHMW), Swedish Museum of Natural History, Stockholm, Sweden (NRM), Landesmuseum Joanneum, Graz, Austria (LMJ), Niederösterreichisches Landesmuseum, Sankt Pölten, Austria (NÖLM), Naturmuseum Senckenberg, Frankfurt/Main, Germany (SMF), naturalis National Museum of Natural History, Leiden, The Netherlands (NNM), and Bayerische Staatssammlung für Paläontologie und Geologie, Munich, Germany (BSPG). Abbreviations are also used in the figure captions, indicating in which collections the specimens and slides are stored. 3. Descriptions and systematic palaeontology The terminology used for bennettitalean reproductive parts varies considerably. To avoid confusion, we follow the general terminology applied by Watson and Sincock (1992), and use the term “flower” for the whole reproductive structure and “perianth” for the surrounding bracts or scale leaves (involucrum) despite the ordinary referral of these terms to angiosperms. However, we refrain from using other terms that specifically refer to angiosperm structures or organs, but rather use the more informal terms “seed cone” (instead of “fruit”), “outer surface” (instead of “pericarp”), and refer to the female structure as “ovulate organ” (and not “gynoecium”) to avoid confusion since, for instance, “gynoecium” refers to the female part of the flower in general, but does not distinguish between mature or immature stages as do “seed cone” and “ovulate organ”. For stomatal morphology we use the term “(brachy)paracytic stomata”, which is defined based on architecture of the stomatal apparatus (Martens,

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1971; Crane, 1988; LAWG, 1999), rather than the ontogeny-based term “syndetocheilic stomata” (Thomas and Bancroft, 1913; Florin, 1933a).

brachyparacytic, with two subsidiary cells, guard cells with prominent, crescent-shaped dorsal thickenings.

Order Bennettitales Engler, 1892. Family Williamsoniaceae Carruthers, 1870.

Description and interpretation: The binominal Cycadolepis wettsteinii is used for isolated, leaf-like organs, which we interpret as detached involucral bracts. Bracts are up to 5.2 cm long and 3.9 cm wide, coriaceous and entire-margined, and have a circular to lanceolate or elliptical outline and delicate parallel venation. The apex is abruptly acuminate (Plate I, 2), while the base is truncate and displays a distinct abscission zone/layer. Bracts are convex on one surface and concave on the other. Densely spaced transverse and longitudinal wrinkles occur on the outer surface of the central part of the lamina (Plate I, 1, 4). Based on the preservation and orientation of the fossils, as well as the orientation of the abscission zone, pattern of wrinkles and distribution of stomata, the concave side is interpreted as adaxial and the convex side as abaxial. The epidermis is composed of polygonal to rectangular cells 40– 70 µm long and 15–38 µm wide (Plate II, 1–2). Differentiation between costal and intercostal fields is distinct. Anticlinal and periclinal cell walls are straight and the cuticles lack ornamentation. Stomata are regularly distributed (Plate II, 1), but not arranged in distinct rows. Stomatal density is distinctly higher on one side (the inferred abaxial side). Stomata are brachyparacytic (Plate V, 4), 30–45 µm long and 20–25 µm wide. Stomatal pores (18–23 µm long) are orientated perpendicularly to the veins, but deviation from this orientation may occur. Two rectangular lateral subsidiary cells partly overarch the pit mouth, thereby forming a slightly sunken stoma. The dorsal walls of the reniform guard cells possess heavily cutinised, crescent-shaped central parts, while the polar ends are weakly cutinised (Plate II, 2). Subsidiary cells are often slightly weaker cutinised than the normal epidermal cells. Papillae or trichome bases are absent. The trichome bases mentioned by Kräusel (1949) probably represent preservational artefacts. Kräusel (1949) did not speculate on the affinities of Cycadolepis wettsteinii. Rather, he acknowledged the differences between Euryand Dory–Cycadolepis, two taxa that were introduced as sub-genera of Cycadolepis by Seward (1917: p. 494–496). Based on Seward (1917), Harris (1969) emended the generic diagnosis for Cycadolepis by expanding the range of leaf shapes (lanceolate to circular) included in that genus. Harris (1969) regarded C. villosa (de Saporta, 1874: p. 201, pl. 114, fig. 4) as the type of the genus. Moreover, he suggested that the affinities of Cycadolepis lie with the Bennettitales, despite the fact that cuticles of the genotype specimen had not been described. Harris (1932, 1969) subsequently interpreted Cycadolepis scale leaves similar to C. wettsteinii as parts of a caducous bennettitalean involucre that surrounded the ovulate structures in female flowers and the whorls of pollen organs in bisexual flowers [for example, see restorations of Williamsoniella coronata Thomas in Harris (1969: text-fig. 61A), and other reconstructions in Watson and Sincock (1992: text-fig. 5B–C, M)]. Cycadolepis wettsteinii bracts are sufficiently large (up to 5 cm long) to enclose both a developing and immature ovulate structure [the mature seed cone, possibly still growing during maturation of the seeds, is up to 9 cm in diameter; cf. also Watson and Sincock (1992)] as well as the whorl of pollen organs prior to pollination. The bracts perhaps formed a protective enclosure for the developing bud (Harris, 1932) and were shed at anthesis. On

Genus Cycadolepis Saporta, 1874 emend. Harris, 1969. Diagnosis: Scale leaves of rather large size, shape varying from lanceolate to circular, margin entire, surface concave on one side, convex on the other; cuticle where known different on the two sides, stomata with syndetocheilic [brachyparacytic] subsidiary cells opposite each guard cell (Harris, 1969). Type species: Cycadolepis villosa Saporta, 1874 (p. 201, pl. 114, fig. 4). Cycadolepis wettsteinii Kräusel, 1949 emend. Plates I, 1–4; II, 1–2; V, 4 Synonyms: 1917 ?Williamsonia wettsteinii in part — Krasser, Studien Mikrosporophylle, p. 491, 549 (nomen nudum). 1949 Cycadolepis wettsteinii — Kräusel, Koniferen und Gymnospermen Lunz, p. 62–65, pl. 14, figs 1–7; pl. 15, figs 4–13; pl. 16, figs 1–2. Holotype: GBA 2006/004/0005 (Plate I, 3). Paratypes: NHMW 1885/D/3974, 1885/D/4104, 1885/D/4116, 1885/D/ 4117, 1885/D/4119, 1885/D/4120, 1885/D/4121, 1885/D/4127 (figured in Kräusel, 1949). Remarks: The species Cycadolepis wettsteinii was formally established by Kräusel (1949) based on material from Lunz that was in part studied by Krasser (1917) and referred to as ?Williamsonia wettsteinii. Krasser (1917) also included in ?Williamsonia wettsteinii several specimens that are here described as Bennetticarpus wettsteinii. Kräusel (1949) designated the specimen GBA 2006/ 004/0005 (originally labelled Williamsonia juvenilis by Krasser) as the holotype for C. wettsteinii (Kräusel, 1949: pl. 15, fig. 4). In addition, several specimens kept in the NHMW collection were regarded as isotypes of C. wettsteinii (Kräusel, 1949: p. 62–63, textfig. 12 b–c, e–h, k, m–n; pl. 14, fig. 1–2; pl. 15, fig. 5–10, 12–13). According to the ICBN (McNeill et al., 2006), however, these specimens in fact represent paratypes. Cuticles were illustrated by Kräusel (1949: pl. 14, figs 3–7), but we cannot determine from which of the specimens the cuticles were obtained. Repository of type specimens: Palaeobotanical collections of the Geological Survey of Austria, Vienna, and the Museum of Natural History, Vienna. Material: 31 specimens from the following collections: NHMW, GBA, NNM and NRM. Emended specific diagnosis: Scale leaves (bracts) of circular to lanceolate shape, slightly concave, apex abruptly acuminate, base truncated, with transverse and longitudinal wrinkles on outer surface; epidermal cells polygonal, anticlinal cell walls straight; stomata small, Plate I. Macromorphology of Cycadolepis wettsteinii and Haitingeria krasseri. 1. 2. 3. 4. 5. 6. 7. 8. 9.

Cycadolepis wettsteinii scale leaf, specimen NHMW 1885/D/4116, paratype; note the wrinkles on the surface. Cycadolepis wettsteinii, specimen NHMW 1885/D/4117, paratype; note the small spiny apex. Cycadolepis wettsteinii scale leaf, specimen GBA 2006/004/0005, holotype. Detail of wrinkles on the surface of Cycadolepis wettsteinii, specimen NHMW 1885/D/4119, paratype. Haitingeria krasseri pollen organ, BSPG (without number). Haitingeria krasseri pollen organ, note the bent segments and pollen sacs (arrows), specimen LMJ 63865. Haitingeria krasseri pollen organ, note the bent segments and attached pollen sacs, specimen NRM S148563 (arrows indicate pollen sacs). Haitingeria krasseri pollen organ, note the bent segments with attached pollen sacs, specimen GBA 1919/002/0001, lectotype. Detail of segments of Haitingeria krasseri with attached pollen sacs (arrows), specimen GBA 1919/002/0001, lectotype. Scale bars are 10 mm in all figures.

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the other hand, the bracts may have served as pollinator attractants of the anthetic (bisexual) flower and were only shed after pollination. The latter was, however, questioned by Harris (1973). It is generally assumed that the male flowers of unisexual Williamsoniaceae did not produce Cycadolepis bracts (Harris, 1969). A conspicuous feature of many Cycadolepis specimens, including most C. wettsteinii specimens from Lunz, is transverse wrinkles (Plate I, 4), which appear to have formed post mortem, perhaps as a result of shrinkage of the subepidermal tissues (Harris, 1969). The exact mechanism(s) leading to this shrinkage remain unknown. It is possible that withering of the disarticulated leaves played a role in that process. Comparisons: Although the morphology of the Cycadolepis wettsteinii specimens from Lunz generally concurs with the definition of Cycadolepis by Harris (1969), only C. hallei Harris (Harris, 1969) from the Liassic of Yorkshire is morphologically similar to C. wettsteinii. The generic diagnosis for Cycadolepis excludes scale leaves accommodated in Deltolepis Harris that are of cycadalean affinities (i.e., stomatal morphology), in spite of the fact that several Deltolepis specimens figured and described by Harris (1964) appear to be more similar morphologically to C. wettsteinii than to certain forms in Cycadolepis. Other scale leaves comparable to C. wettsteinii have been reported by Watson and Sincock (1992) and Boyd (2004) from the Lower Cretaceous of the southern U.K. and West Greenland. Genus Haitingeria Krasser, 1919 emend. Kräusel, 1949 Emended diagnosis: Lanceolate to broadly oval, ±laminar imparipinnate pollen organ (microsporophyll), shed after pollen dispersal, lateral margins dissected into short segments bearing pollen sacs, sporangia single (free); epidermal cells polygonal, anticlinal cell walls straight; stomata small, brachyparacytic, with two subsidiary cells; guard cells with prominent, crescent-shaped dorsal thickenings; pollen sacs fusiform, round or oval in outline, borne individually in a row on adaxial side of segments, [emended after the original Latin and German diagnoses in Krasser (1919a) and Kräusel (1949)]. Type species: Haitingeria krasseri (Schuster, 1911) Krasser, 1919 (p. 2–7, pl. 1, fig. 1). Haitingeria krasseri (Schuster, 1911) Krasser, 1919 emend. Plates I, 5–9; II, 4–7; V, 3; VI, 1, 5 Synonyms: 1909 Cycadospadix sp. — Krasser, Kenntnis Flora Lunzer Schichten, p. 114 (no illustration). 1911 Cycadospadix krasseri — Schuster, Weltrichia und die Bennettitales, p. 51, pl. 5, fig. 11. 1916 Haitingeria krasseri (Schuster) — Krasser, Studien Mikrosporophylle, p. 336 (nomen nudum). 1917 Haitingeria krasseri (Schuster) — Krasser, Studien Mikrosporophylle, p. 490 [2] (nomen nudum). 1919 Haitingeria krasseri (Schuster) — Krasser, Studien Makrosporophylle, p. 2–7, pl. 1. 1931 Haitingeria krasseri Schuster — Schuster, Verhältnis Cycadeen, p. 190 (no illustration).

1949 Haitingeria krasseri (Schuster) Krasser — Kräusel, Koniferen und Gymnospermen Lunz, p. 49–55, pl. 9, figs 8–9; pl. 10, figs 8–11; pl. 11, figs 1–4. Lectotype: GBA 1919/002/0001 (Plate I, 8). Epitype: NHMW 1885/D/4123 (Plate VI, 1). Remarks: The species was first described as Cycadospadix krasseri by Schuster (1911) based on specimens from Lunz. One specimen was illustrated (Schuster, 1911: pl. 5, fig 11), and thus serves as the holotype. Krasser (1916, 1917, 1919a) restudied the fossils and transferred the species to a new genus, Haitingeria, that was formally introduced by Krasser (1919a), probably in order to underline the clear distinction from recent and extinct Cycas L. and Cycas-like macrosporophylls (Krasser, 1919a: p. 13). The holotype of Schuster (1911) was kept in the collection of the BSPG in Munich, but was probably destroyed during World War II. The designation of a lectotype is therefore required (ICBN Art. 9.2 in McNeill et al., 2006). Krasser (1919a) illustrated several compression specimens of Haitingeria krasseri from Lunz together with cuticle preparations showing distinct bennettitalean epidermal features. It remains unclear from which of the specimens the cuticles were obtained. We designate specimen GBAW 1919/002/ 0001 [originally figured by Krasser (1919a: pl. 1, fig. 1); here refigured as Plate I, 8] as the lectotype of H. krasseri mainly because of its good preservation showing several specific details. However, cuticles cannot be obtained from this specimen because it is varnished. To acknowledge the bennettitalean nature of H. krasseri, we designate as the epitype the specimen NHMW 1885/D/4123, which has well-preserved cuticles showing distinctive bennettitalean epidermal features that are similar to features illustrated by Kräusel (1949). Haitingeria krasseri also serves as the type species of the genus Haitingeria. Repository of holotype and epitype: Palaeobotanical collections of the Geological Survey of Austria, Vienna, and the Museum of Natural History, Vienna. Material: 24 specimens from the following collections: NHMW, GBA, NRM, LMJ and SMF. Emended specific diagnosis: Pollen organ (microsporophyll), shed after pollen dispersal; imparipinnate; lanceolate to broadly oval in outline, apex obtuse, lateral margins dissected into short segments bearing pollen sacs; segments increasing in length towards apex; epidermal cells polygonal, anticlinal cell walls straight; stomata small, brachyparacytic, with two subsidiary cells; guard cells with prominent, crescent-shaped dorsal thickenings; pollen grains monosulcate. Description and interpretation: The morphotaxon Haitingeria krasseri is used for isolated pollen organs. The fact that these fossils consistently occur isolated indicates that the sporophylls were shed after pollen dispersal. Sporophylls are up to 9.2 cm long and 6.3 cm wide, lanceolate to broadly-oval in outline, marginally imparipinnate with obtuse apex and truncate base (Plate I, 5–9). The central portion of the pollen organ displays several delicate veins extending from the base to the lateral margins. In the upper two thirds of the sporophyll, the lateral margin is dissected to form 4–10 segments, each up to 2 cm

Plate II. Cuticles of Cycadolepis wettsteinii, Haitingeria krasseri and Nilssoniopteris angustior (note the correspondence in stomatal morphology in all three taxa). 1. 2. 3. 4. 5. 6. 7.

Abaxial cuticle of Cycadolepis wettsteinii, overview with stomata in intercostal fields, slide NHMW 1885/D/4127/0003. Detail of abaxial cuticle of Cycadolepis wettsteinii with several brachyparacytic stomata, slide NHMW 1885/D/4127/0003. Abaxial cuticle of Nilssoniopteris angustior, middle portion of the lamina, epidermal cells with papillae on left side of image, cells without papillae on right side of image, slide NHMW 1884/0015/0010. Haitingeria krasseri, abaxial cuticle of the laminar part of the sporophyll with several brachyparacytic stomata arranged in intercostal fields, slide NHMW 1885/D/3935/0004. Detail of abaxial cuticle of Haitingeria krasseri, slide NHMW 1885/D/3935/0004. Adaxial cuticle of Haitingeria krasseri with papillate epidermal cells, slide NHMW 1885/D/4026/0014. Adaxial cuticle of Haitingeria krasseri, slide NHMW 1885/D/4026/0013. Scale bars are 100 µm in all figures.

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long (Plate I, 5–8). Segment length increases towards the apex. Some of the specimens possess segments that seem to be curved in an inward direction (Plate I, 6–8). Each of the segments bears at least ten oval to lanceolate pollen sacs (Plate I, 6–9). The epidermis of the central part of the lamina is composed of polygonal to rectangular cells, 35–65 µm long and 18–38 µm wide (Plate II, 4–5). Costal and intercostal fields clearly differ with regard to the epidermal cell pattern (Plate II, 4). Anticlinal and periclinal cell walls are straight; a surface ornament is absent. Stomata occur regularly scattered in the intercostal fields (Plate II, 4). Stomatal density is distinctly higher on the adaxial side (Kräusel, 1949). Stomata are brachyparacytic, 38–48 µm long and 15–23 µm wide; the pores (18–20 µm) are orientated parallel to the veins. Two rectangular subsidiary cells partly overarch the pit mouth and form a slightly sunken stoma. The dorsal walls of the reniform guard cells have heavily cutinised, crescent-shaped central parts, whereas the polar ends are only weakly cutinised (Plates II, 5; V, 3). Subsidiary cells are often weaker cutinised than the normal epidermal cells (Plates II, 5, 7; V, 3). Papillae and trichome bases have not been observed, but small central thickenings occur on the periclinal walls of the epidermal cells of the adaxial surface (Plate II, 6). Pollen sacs are elongate–elliptical in outline and up to 3 mm long. They are borne on the adaxial side of the segments (Plate I, 7–9), apparently arranged in a single row (Plate I, 7, 9) in the lateral segments. Pollen grains are oval in outline, 120–160 µm in diameter, and are monosulcate (cf. Kräusel, 1949). Unfortunately, cuticle remains interpreted as belonging to pollen sacs were not found in organic connection to epidermal cuticle from Haitingeria sporophylls. Schuster (1911), in his first account on Cycadospadix krasseri, described the fossils as “Cycas-like sporophyll”, but did not specify whether the sporophylls were female or male. Krasser's (1919a) description of Haitingeria krasseri suggests that they are megasporophylls bearing seeds along the segmented outer margin. However, Schuster (1931) and Harris (1932) questioned this interpretation, and Harris (1932) compared H. krasseri with Bennettistemon amblum Harris, a pollen-producing organ from the Rhaetian of Greenland. Kräusel (1949) suggested that H. krasseri is microsporangiate, and documented the presence of abundant pollen grains on the surface of the structures (Kräusel, 1949: p. 52–53). Moreover, Kräusel (1949) documented the syndetocheilic (paracytic) stomatal morphology for H. krasseri, and consequently assigned the fossils to the Bennettitales. He suggested that H. krasseri may be similar to a “male Williamsonia Carruthers flower with particular stamina” or “a male part of a bisexual flower” (Kräusel, 1949: p. 53). Moreover, he studied the morphology and epidermal anatomy of Bennetticarpus wettsteinii (see below). Although he suggested that B. wettsteinii and H. krasseri may belong to the same plant, he did not formally propose unification of the two taxa. Comparisons: Haitingeria pollen organs are distinguished from all other known bennettitalean pollen organs by their palmate, ±laminar outline with segments that are not coiled or folded and by the single row of pollen sacs per segment. The only other specimen referred to the genus is H. rajmahalensis Feistmantel (Feistmantel, 1877; Wieland, 1916; Krasser, 1919a), a palmate, laminar pollen organ from the Early Cretaceous of India that is characterised by a reduced central laminar part (Wieland, 1916: p. 205, text-fig. 81B).

However, little information is available about this fossil; we are aware of only the schematic illustrations in Feistmantel (1877) and Wieland (1916), and a single, cryptic photograph in Krasser (1919a: pl. 1, fig. 10). None of these illustrations permits a more detailed comparison to H. krasseri. Consequently, the incompletely known H. rajmahalensis should better be excluded from the genus. Kräusel (1949) excluded all other specimens assigned or related to Haitingeria by Krasser (1919a) and Schuster (1931) based on the apparent ovulate nature of these fossils. Recently, specimens assigned to H. cf. krasseri were described from the Upper Triassic of Sonora, Mexico (Weber, 2008). These leaves represent the first report of persuasive Haitingeria-like microsporophylls beyond the Lunz flora; the leaves from Mexico are somewhat smaller, but have an outline rather similar to H. krasseri from Lunz. Haitingeria krasseri shows some resemblance to the pollen organs of Weltrichia mexicana Wieland from the Liassic of Oaxaca, Mexico (Wieland, 1916: p. 171, 203–205, text-fig. 81E), W. spectabilis (Nathorst) Harris from the Middle Jurassic of Whitby and Marske Quarry, Yorkshire, U.K. (Nathorst, 1909: p. 6–8, pl. 1, fig. 1; Nathorst, 1911: p. 5–8, pl. 1, figs 1–11, pl. 3, fig. 1; Thomas, 1913, p. 230–232, pl. 24, figs 1a–3; Harris, 1969: p. 166–168, pl. 7, fig. 8), and W. mirabilis Braun from the Liassic of Bayreuth, Germany (Braun, 1849: e.g., pl. 2, fig. 3; Schuster, 1911: pl. 6, fig. 3). Correspondences between the taxa include the elongate triangular, planate form and the position of the pollen sacs. However, in all of these species of Weltrichia Braun the pollen organs are basally fused. Harris (1969) discussed several of the species and suggested reconstructions for three other species [i.e., W. setosa (Nathorst) Harris, W. sol Harris and W. whitbiensis (Nathorst) Harris]. However, the individual pollen organs of the latter forms differ from H. krasseri in lacking a pinnate architecture and in having synangiate pollen sacs. Morphogenus Bennetticarpus Harris, 1932 Definition: “This designation is intended for all gynoecia with definitely bennettitalean characters, which are not fully enough known to be included in or definitely separated from the existing genera” (Harris 1932, 1969). Type species: Bennetticarpus oxylepidus Harris, 1932 (p. 101, pl. 14, figs 1–6, 11; text-figs 48D–F). Bennetticarpus wettsteinii (Krasser, 1912) Kräusel, 1949 Plates III, 1–8; IV, 1–6; V, 1 Synonyms: 1909 Williamsonia sp. — Krasser, Kenntnis Flora Lunzer Schichten, p. 114 (nomen nudum). 1912 Williamsonia wettsteinii — Krasser, Williamsonia in Sardinien, p. 955, pl. 2, fig. 9. 1916 Williamsonia wettsteinii Krasser — Krasser, Studien Mikrosporophylle, p. 337 [3], (no illustration). 1917 Williamsonia wettsteinii Krasser — Krasser, Studien Mikrosporophylle, p. 491, 549 (no illustration). 1933 Williamsonia wettsteinii Krasser — Florin, Die Spaltöffnungsapparate, p. 8, pl. 1, fig. 1, text-fig. 2.

Plate III. Macromorphology of Bennetticarpus wettsteinii. 1. 2. 3. 4. 5. 6. 7. 8.

Seed cone with seeds and seed scales in the left part, view from above, originally figured in Krasser (1917), specimen GBA 1917/001/0026, holotype. Seed cone with excellently preserved outer surface, specimen NHMW 1889/VI/13. Seed cone with excellently preserved outer surface, specimen NRM S148325, epitype. Detail of the outer surface giving an idea about the carnose nature of the cone figured in Plate III, 3, specimen NRM S148325, epitype. Detail of the outer surface with hexagonal shields interpreted as apices of interseminal scales, specimen GBA 1917/001/0029. Detail of the hexagonal tips of the interseminal scales, specimen NÖLM F/0072, figured also in Plate III, 8. Detached scales, one bearing a seed, specimen NHMW 1883/C/595. Seed cone with possible abscission scar (arrow), specimen NÖLM F/0072. Scale bars are 10 mm in Figs 1–4, 8, and 5 mm in Figs 5–7.

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1949 Bennetticarpus wettsteinii (Krasser) — Kräusel, Koniferen und Gymnospermen Lunz, p. 55–61, pl. 11, figs 5–10, pl. 12, figs 1–5, pl. 13, figs 1–6, pl. 15, fig. 1, text-figs 9–11. Holotype: GBA 1917/001/0026 (Plate III, 1). Epitype: NRM S148325 (Plate III, 3). Remarks: The specimen GBA 1917/001/0026, originally described and figured by Krasser (1912: p. 55, pl. 1, fig. 9), is regarded as the holotype. Kräusel (1949) erroneously regarded this specimen as a lectotype. We designate NRM S148325 as an epitype because its cuticles display typical bennettitalean brachyparacytic stomata (figured by Florin, 1933b: pl. 1, fig. 1). Krasser (1912) only briefly described Bennetticarpus wettsteinii under the name Williamsonia wettsteinii; also his synoptical studies of reproductive organs from Lunz do not include a more in-depth consideration of this taxon (Krasser, 1916, 1917). Florin (1933b) later documented the epidermal anatomy of B. wettsteinii, including features that can be used to establish the bennettitalean affinity. The first detailed description of the macromorphology and epidermal anatomy of B. wettsteinii was given by Kräusel (1949). However, this work lacks a valid diagnosis. Kräusel's interpretation of the “cones” remains vague. Moreover, it remains uncertain how Kräusel understood the term “scale”. Kräusel (1949) transferred the species to the genus Bennetticarpus sensu Harris (1932). Repository of types: Palaeobotanical collections of the Geological Survey, Vienna, and the Swedish Museum of Natural History, Stockholm. Material: 23 specimens from the following collection: GBA, NHMW, NRM and NÖLM. Specific diagnosis: Seed cone, apparently spherical in shape at maturity, apex obtuse and rounded, base truncate with abscission scar; outer surface composed of hexagonal shields; anticlinal cell walls of epidermal cells weakly cutinised in the centre of the shields, but heavily cutinised close to the outer margin; stomata brachyparacytic; broadly ovate seeds attached to the central axis, arranged radially; each seed with an inner probably hard part and an outer fleshy zone; weakly cutinised, with an outer cuticular layer comprised of isodiametric and polygonal cells, and a central tubular cylinder spanning from one polar end to the other; tubular cylinder composed of polygonal cells, lumina of cells in the centre of the cylinder contain opaque bodies of uncertain affinity [emended from the German description by Kräusel (1949)]. Description and interpretation: Bennetticarpus wettsteinii is a female reproductive organ in the stage of seed maturity (seed cone). Compression fossils have a circular outline and suggest that the cone was spherical in vivo. The fossils are up to 9 cm in diameter, and have a rounded apex (Plate III, 1–3); the base is rounded with a small abscission scar (Plate III, 8). The outer part of the cone is composed of a thick coaly layer covering the internal structures, including seeds. The outer surface is characterised by numerous laterally fused hexagonal shields, each between 700 and 900 µm in diameter (Plate III, 2–6), with a slightly raised central part (Plate III, 5). The shields, which are recognisable in hand specimens and cuticle preparations, represent the distal ends of the interseminal scales. Rough calculation revealed that there were up

to 30,000–35,000 interseminal scales, given the fruit was spherical and with a diameter of 8–9 cm. Seeds are broadly ovate in outline, up to 13 mm long (Plate III, 7), and arranged in a radiating pattern from the centre. Bennetticarpus wettsteinii seed cones produced c. 25–30 seeds. The receptacle is not visible in any of the specimens (e.g., Plate III, 1). The raised central portion of the seeds is about 4–8 mm long and has a smooth surface, which we interpret as the outer surface of a rigid sclerenchyma layer. This part of the seed is surrounded by a flattened outer zone that we interpret as imprints of an outer fleshy layer (Plate III, 7); consequently, whole seeds could be up to 13 mm in length. There is no direct evidence for seed stalks, but the position of the seeds within the seed cone indicates that the seeds were stalked rather than sessile on the receptacle. The epidermal cells of the hexagonal shields are small and isodiametric, 20–48 µm long and 15–22 µm wide (Plate IV, 1–3). The anticlinal walls of the epidermal cells along the outer margin of the shields are heavily cutinised, but cutinisation gradually decreases towards the centre of the shields (Plate IV, 2–3, 5). Up to twelve brachyparacytic stomata (40–50 µm long and 25–28 µm wide) are irregularly distributed on each shield (Plate IV, 3–4). The two rectangular subsidiary cells are weaker cutinised than the normal epidermal cells and form a slightly sunken stoma (Plate IV, 6). Stomatal pores (15–23 µm) are orientated radially within each shield (Plate IV, 2–3). The dorsal walls of the reniform guard cells have heavily cutinised, crescent-shaped central parts, while the polar ends are weakly cutinised. The seeds (Plate V, 1) are weakly cutinised, with an outer cuticular layer (probably from the raised, sclerenchyma part seen in the macrofossils) comprised of isodiametric polygonal cells, 35–58 µm in diameter. In the centre of the seeds, a tubular cylinder (up to 400 µm in diameter) composed of polygonal cells extends from the base almost to the apex (Plate V, 1). This structure is interpreted as a basally attached nucellus, perhaps conjoined with remnants of the cotyledons (Wieland, 1920: p. 168, fig. 5). The cells of this inner layer contain opaque bodies of unknown affinity that usually fill nearly the entire lumen. The seed in cuticular preservation illustrated in Plate V, 1 is only about 1.5 mm long, but several larger seeds, i.e. up to 6 mm long, obtained from bulk macerations can be assigned to Bennetticarpus wettsteinii as well based on morphological similarities to the seeds obtained from macerated samples. The raised central part of the seed seen in compression fossils is about 4–8 mm long. This suggests that the cuticles illustrated all occur inside the hard sclerenchyma layer, which itself is then surrounded by the outer fleshy layer. If this is correct, then both the hard sclerenchyma layer and fleshy layer represent the inner and outer seed “envelope” sensu Friis et al. (2009) — and this structure is quite similar to that seen in other Bennettitales, according to Friis et al.'s (2009) interpretation. Evidence for a carnose nature of the seed cone occurs in the form of a distinct layer of anthracite (Plate III, 2, 4) that not only covers the surface, but also encloses the seeds (cf. Krasser, 1912; Crane, 1988). Interseminal scales are generally swollen distally (cf. Bose, 1968; Watson and Sincock, 1992), and probably contributed to the carnose nature of the mature seed cone (Plate III, 2–5; see also Vardekloeftia Harris; Pedersen et al., 1989). The openings of the micropylar projections are virtually invisible. This apparent absence of micropyles or micropylar tubes had already been noted by Kräusel (1949; cf. also Crane, 1988). The openings in the surface may have been reduced or closed during seed maturation. In seed cones from younger deposits,

Plate IV. Cuticles of Bennetticarpus wettsteinii. 1. 2. 3. 4. 5. 6.

Cuticle of the outer surface, overview, note regularly arranged hexagonal shields with weaker cutinised central parts, slide GBA 1909/002/0518/0008. Detail of the cuticle of the outer surface with brachyparacytic stomata arranged radially, slide GBA 1909/002/0518/0008. Detail of heavily cutinised border between hexagonal shields, slide GBA 1909/002/0518/0009. Cuticle of outer surface with two stomata, slide GBA 1909/002/0518/0008. Cell pattern close to the border of a hexagonal shield, slide GBA 1909/002/0518/0008. Close-up of a stoma of Bennetticarpus wettsteinii, slide GBA 1909/002/0518/0008. Scale bars are 200 μm in Fig. 1, 100 μm in Figs 2–3, and 25 μm in Fig. 4–6.

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micropylar tubes are well discernible as illustrated e.g., in Bose (1968), Harris (1969) and Crane (1985). Bennetticarpus diodon Harris from the Jurassic of Yorkshire shows evidence for micropyles between the interseminal scales (Harris, 1969; Crane and Herendeen, 2009). Cuticles from a species of Williamsonia from the Upper Triassic Chinle Formation (Ash, 1968) also show evidence for the presence of micropyles and micropylar tubes penetrating the surface of the ovulate organ. Moreover, both reproductive organs have interseminal scales with an epidermal anatomy almost identical to that of B. wettsteinii. Vardekloeftia also shows distinct micropyles (Pedersen et al., 1989). On the other hand, Harris (1969) mentioned two species of Bennetticarpus from the Jurassic of Yorkshire, i.e., B. fragum Harris and B. litchi Harris, in which micropyles are not visible on the surface. Harris (1969) compared at least B. litchi with B. wettsteinii. In almost all bennettitalean ovulate structures, micropyles persist at the surface throughout. This also appears to be the case in some specimens of Cycadeoidea Buckland ex Lindley et Hutton in which the seeds are known to be mature because of the presence of dicotyledonous embryos. Bennetticarpus wettsteinii may be unusual in this respect. In B. wettsteinii perhaps the micropyles were exposed initially, but upon pollination became obscured by enlargement or proliferation of the interseminal scales. In general, Bennetticarpus wettsteinii is morphologically comparable to other bennettitalean ovulate cones that possess a central receptacle bearing stalked ovules alternating with interseminal scales (see e.g., Harris, 1932, 1969; Watson and Sincock, 1992). However, it represents one of the earliest bennettitalean reproductive structures. It is closer to Vardekloeftia sulcata Harris from the Upper Triassic of Greenland (Pedersen et al., 1989) than to other, younger bennettitalean seed cones. Vardekloeftia sulcata is a form that possesses hexagonal shields very similar to those of B. wettsteinii, not only with regard to size, but also epidermal anatomy and stomatal distribution. Although V. sulcata is distinctly smaller, both forms represent seed cones of early bennettitaleans that have in common a low number of relatively large seeds, combined with a large number of interseminal scales. 4. Discussion 4.1. Reassembling the flower parts The three isolated bennettitalean flower parts from the Carnian of Lunz, Cycadolepis wettsteinii, Haitingeria krasseri and Bennetticarpus wettsteinii, share several macromorphological and epidermal features, which strongly suggests that they belong to the same flower (reassembled in Figs. 2 and 3; cf. Table 1). Already Kräusel (1949) suggested that C. wettsteinii and H. krasseri were produced by the same reproductive structure comprising an outer whorl of sterile bracts (C. wettsteinii), an inner whorl of pollen organs (H. krasseri) and a central ovulate structure. Bracts and pollen organs were shed at maturity. In addition, Kräusel (1949) believed that B. wettsteinii represented the seed cone (“fruit”) of this flower. Cycadolepis wettsteinii and Haitingeria krasseri are similar in size and overall shape; both have a broad, well-defined and slightly concave abscission scar. Structural differences between C. wettsteinii and H. krasseri can be explained by the different functions of these organ types (scale leaf vs. pollen organ). Moreover, C. wettsteinii and H. krasseri share several epidermal features, including the size, morphology and arrangement of the normal epidermal cells and the brachyparacytic stomata (Table 1). Similarities in epidermal anatomy

also link the seed cones of Bennetticarpus wettsteinii to C. wettsteinii and H. krasseri. All have stomata that are slightly sunken and subsidiary cells that are less heavily cutinised than the normal epidermal cells. Also the cutinisation pattern of the guard cells is similar in all three taxa (i.e., the dorsal walls of the guard cells and the crescent-shaped central parts are heavily cutinised, whereas the polar ends are weakly cutinised; Plate V, 2–4; Table 1). The walls of the epidermal cells are smooth in all taxa, and papillae and trichomes are absent. Finally, all three organ types occur in relatively high numbers in the Lunz flora and in several instances co-occur on the same slabs (e.g. Plate VI, 5). Further, they are far more abundant at the Lunz locality than any other seed plant reproductive organ. The only difference in epidermal anatomy between the three taxa is that the epidermal cells of B. wettsteinii are smaller and the cell walls more heavily cutinised than in C. wettsteinii and H. krasseri, but this can be explained by the production of a carnose outer layer during seed maturation. It is also important to note that the stomata of the three organ types described here are more similar to each other than to the stomata of any other bennettitalean fossil from the Lunz locality [for details on the anatomy of for example Pterophyllum Brongniart leaves from Lunz, see Pott et al. (2007b)]. Abscission scars in Cycadolepis wettsteinii and Hatingeria krasseri are 10–13 mm wide. Cycadolepis bracts are known to occur in the female flowers of the unisexual bennettitaleans and in bisexual flowers (cf. Harris, 1969). Consequently, a similarly large abscission scar in H. krasseri pollen organs suggests that a larger structure requiring this large diameter must have existed in the centre of the flower. Abscission scars in C. wettsteinii and H. krasseri correspond well with the estimated diameter of the axis of the Bennetticarpus wettsteinii (Fig. 3) seed cone that is calculated at approximately 20 mm based on the scar seen in one specimen (Plate III, 8) and comparisons with other bennettitalean reproductive structures figured in Watson and Sincock (1992). It also corresponds well to the dimensions seen in other plants that have a large, heavy ovulate/fruiting structure, e.g., Magnolia grandiflora L. (Catesby, 1738; Vázquez-Garcia, 1994). The individual parts of the reassembled flower (Figs. 2 and 3) consistently occur as isolated fossils, appear to be fossilised at the stage of maturity, and show distinct abscission regions. This, together with clear evidence of withering (e.g., wrinkles on the surfaces, distorted cell walls), indicates that the individual parts were shed after maturation. As a result, the chance of finding these organ types in organic connection is probably low. Only mature ovulate (seed) cones have been discovered to date. We interpret this fossil flower as bisexual (Fig. 2) despite the fact that this stands in contradiction to the general view that early bennettitalean flowers were unisexual (Crane, 1985, 1988). Although it cannot be ruled out that the three organ types were produced by unisexual flowers, rather than bisexual flowers, we hold the opinion that the following aspects argue against unisexual flowers: (A) Rather wide abscission scars in both Haitingeria krasseri and Cycadolepis wettsteinii are suggestive of the presence of a robust axis with a considerable diameter and a large structure in the centre of the flower (Fig. 2). A robust central axis may be necessary to support the large and, at maturity, probably heavy ovulate cone (Fig. 3). (B) Haitingeria krasseri pollen organs and Cycadolepis wettsteinii bracts are free for their whole length and were apparently shed

Plate V. Cuticular details of Bennetticarpus wettsteinii, Cycadolepis wettsteinii, Haitingeria krasseri and Nilssoniopteris angustior. 1.

Seed of Bennetticarpus wettsteinii in cuticle preservation, slide NHMW 1885/D/4124/0003.

2. 3. 4.

Close-up of a stoma of Nilssoniopteris angustior, slide NHMW 1884/0015/0012. Close-up of a stoma of Haitingeria krasseri, slide GBA 1909/003/0149/0004. Close-up of a stoma of Cycadolepis wettsteinii, slide NHMW 1885/D/4127/0003. Scale bars are 100 μm in Fig. 1, and 10 μm in Figs 2–4.

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Fig. 2. Reconstruction of the bennettitalean flower composed of Cycadolepis wettsteinii bracts, Haitingeria krasseri pollen organs and an assumed central receptacle bearing alternating interseminal scales and stalked ovules. Scale bar 10 mm. Drawing by Polyanna van Knorring, Stockholm.

(C)

(D) (E)

(F)

individually after opening of the flower or after pollination, which implies continued growth of the ovulate organ (Figs. 2 and 3). In bennettitaleans with unisexual flowers, the male flowers always have basally or laterally fused pollen organs united into a cup-like structure that is often shed as a whole, while bennettitalean flowers with free pollen organs are all bisexual [e.g., Harris, 1969; and own observations based on a thorough review of the published record covering the complete stratigraphic range of Bennettitales from the Upper Triassic (Carnian) up to the Lower Cretaceous (Wealden), including fructifications from all over the world (i.e., Mexico, Northern and Southern America, United Kingdom, Greenland, Sweden, Germany, Poland, Austria, Italy, Romania, Iran and Afghanistan, India, China, Australia/Tasmania and Antarctica)]. Isolated female flowers of geologically younger bennettitaleans with unisexual flowers retain their bracts almost until fruit maturation (Harris, 1969; Watson and Sincock, 1992). This feature has not been observed in any seed cone of Bennetticarpus wettsteinii. Correspondences in cuticle/epidermal anatomy strongly suggest that the organs were produced by the same plant. The organs commonly co-occur, not only in the same layer, but also on the same slabs, which supports that these isolated organs were produced by the same plants (Harris, 1969). Nilssoniopteris foliage (see below) is usually associated with plants producing bisexual flowers (Harris, 1969; Crane, 1988; Crane and Herendeen, 2009).

4.2. Linking the flower to sterile foliage Previous studies have used epidermal anatomy of Cycadolepis to link reproductive structures and leaf taxa, e.g., Harris (1969) for C. spheniscus Harris and Otozamites gramineus (Phillips) Harris. Bennettitalean foliage is common in the Lunz flora, and often co-occurs with bennettitalean

Fig. 3. Reconstruction of the Bennetticarpus wettsteinii seed cone; close-up illustrates a detail of the surface. Scale bar 10 mm. Drawing by Polyanna van Knorring, Stockholm.

reproductive organs on the same slabs. The foliage belongs to two different morphogenera, Pterophyllum and Nilssoniopteris Nathorst emend. Pott et al. (Pott et al., 2007a,b). Based on correspondence in several epidermal features to C. wettsteinii and Haitingeria krasseri (e.g., arrangement, size, outline, architecture, and cutinisation of the epidermal cells and stomatal morphology; Plates III, 3; V, 2–4; VI, 6–7; Table 1), the Lunz flower most likely belonged to the plant that produced Nilssoniopteris angustior leaves (Plate VI, 2–5). The reconstructed plant (flower and leaves) presented here is currently known only from Lunz. Organs similar to Haitingeria krasseri and Bennetticarpus wettsteinii have not been found in the coeval and otherwise very similar flora from Neuewelt (Switzerland) or any other locality. Nilssoniopteris foliage is also not reported from Neuewelt (Pott et al., 2007a), whereas other bennettitalean foliage and fertile structures such as two common types of Pterophyllum foliage and Leguminanthus siliquosus (Leuthardt) Kräusel and Schaarschmidt pollen organs are known from both Lunz and Neuewelt (Kräusel and Schaarschmidt, 1966; Pott et al., 2007b). The latter also strengthens the interpretation that the reconstructed plant more likely produced Nilssoniopteris than Pterophyllum foliage. 4.3. Triassic bennettitalean reproductive organs The reconstructed flower presented here would be the first complete bennettitalean flower from the Triassic that has been reassembled from isolated parts, and provides a rare opportunity to discuss early character evolution in the Bennettitales. Most bennettitalean reproductive organs that have been illustrated and/or reconstructed come from the Jurassic or Cretaceous (e.g., Nathorst, 1888; Harris, 1969; Crepet, 1974; Bose et al., 1984; Watson and Sincock, 1992; Stockey and Rothwell, 2003). Reports of well-preserved Triassic ovulate cones and reproductive organs are rare (e.g., Harris, 1932;

Plate VI. Haitingeria krasseri, leaves of Nilssoniopteris angustior. 1. 2. 3. 4. 5. 6. 7.

Epitype of Haitingeria krasseri, specimen NHMW 1885/D/4123. Complete leaf of Nilssoniopteris angustior, specimen NHMW 1887/I/0009. Complete Nilssoniopteris angustior leaf, specimen GBA 1909/002/0187. Nilssoniopteris angustior leaf, specimen NHMW 1885/D/1212. Specimen NRM S148563 with Haitingeria krasseri pollen organ and several Nilssoniopteris angustior leaves (arrows). Adaxial cuticle of Nilssoniopteris angustior without stomata, slide NRM S148231/0001. Abaxial cuticle of Nilssoniopteris angustior with stomata arranged in irregular lines, slide NRM S148231/0001. Scale bars are 10 mm in Figs 1–5, and 100 μm in Figs 6–7.

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Table 1 Synopsis of macromorphological and epidermal features of Cycadolepis wettsteinii, Haitingeria krasseri, Bennetticarpus wettsteinii and Nilssoniopteris angustior. Haitingeria krasseri

Bennetticarpus wettsteinii

Nilssoniopteris angustior

Involucral scale leaf Shed at maturity Entire-margined, lanceolate to elliptical, acute or spiny apex, truncate base

Size Surface/venation

Fruit Shed at maturity Proposed spherical shape, apex obtuse rounded, base truncate; outer surface with “pericarp” Up to 9 cm in diameter n/a

Sterile foliage Unknown Petiolate, narrow, oblong to lanceolate; acute apices; not subdivided into segments, but occasionally growth aberrations of the leaf margin Up to 29.0 cm long and 5.2 cm wide Numerous parallel veins perpendicularly to the midrib

Epidermal cells Size Pattern

Up to 5.2 cm long and 3.9 cm wide Several transverse and longitudinal wrinkles on the outer surface of central part Polygonal to rectangular 40–70 µm long and 15–38 µm wide Costal and intercostal fields are recognisable

Pollen organ Shed at maturity Palmate, imparipinnate, lanceolate to broad-oval, apically obtuse, truncate base; lateral margin is dissected into 4–10 segments Up to 9.2 cm long and 6.3 cm wide Several fine vein courses tracing from the base of the microsporophyll towards the lateral margin Polygonal to rectangular 35–65 µm long and 18–38 µm wide Costal and intercostal fields are recognisable

Small, isodiametric 20–48 µm long and 15–22 µm wide n/a

Cell walls

Smooth, no ornamentation

Smooth, no ornamentation

Stomata

Regularly scattered in intercostal fields

Regularly scattered in intercostal fields

Smooth, no ornamentation, partly strongly cutinised Irregularly scattered in hexagonal fields (“tips” of interseminal scales)

Isodiametric, rectangular 20–70 µm long and 20–42 µm long Costal and intercostal fields are not clearly differentiated; alternation of stomatiferous and non-stomatiferous areas on the abaxial side Smooth, no ornamentation

Type Size Position Guard cells

Syndetocheilic/diacytic 30–45 µm long and 20–25 µm wide Slightly sunken Dorsal walls of guard cells possess strongly cutinised, crescent central parts; polar ends only weakly cutinised Subsidiary cells often slightly less cutinised than normal epidermal cells 18–23 µm long Oriented perpendicularly to veins Absent

Syndetocheilic/diacytic 38–48 µm long and 15–23 µm wide Slightly sunken Dorsal walls of guard cells possess strongly cutinised, crescent central parts; polar ends only weakly cutinised Subsidiary cells often slightly less cutinised than normal epidermal cells 18–20 µm Oriented parallel to veins Absent

Subsidiary cells Stomatal porus Papillae/trichomes

Syndetocheilic/diacytic 40–50 µm long and 25–28 µm wide Slightly sunken Dorsal walls of guard cells possess strongly cutinised, crescent central parts; polar ends only weakly cutinised Subsidiary cells often slightly less cutinised than normal epidermal cells 15–23 µm Oriented radially within a shield Absent

Stomata and subsidiary cells arranged in long rows, orientated perpendicular to the rachis; they alternate with non-stomatiferous bands of cells Syndetocheilic/diacytic 32–45 µm long and 15–25 µm wide Slightly sunken Dorsal walls of guard cells possess strongly cutinised, crescent central parts; polar ends only weakly cutinised Subsidiary cells often slightly less cutinised than normal epidermal cells 13–18 µm Oriented perpendicularly to the veins Long hollow papillae irregularly scattered

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Cycadolepis wettsteinii Proposed function Abscission Lamina

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Kräusel and Schaarschmidt, 1966; Ash, 1968; Pedersen et al., 1989; Anderson et al., 2007), or the nature of the fossils remains incompletely understood [e.g., Williamsonia alpina Krasser from the Triassic of St. Cassian in northern Italy (Krasser, 1919b), Sturiella langeri Kräusel (Kräusel, 1948; but see Friis and Pedersen, 1996), Pramelreuthia haberfelneri Krasser (Kräusel, 1949; Ash and Litwin, 1996), Westersheimia pramelreuthensis Krasser (Kräusel, 1949) from the Carnian of Lunz, and Williamsonianthus keuperianus Kräusel and Schaarschmidt from the Carnian of Neuewelt, Switzerland]. Moreover, the Triassic record mostly consists of disarticulated parts with little or no information pertinent for reconstruction of the organisation of the flowers (Krasser, 1917, 1919a,b; Harris, 1932; Kräusel, 1948, 1949; Kräusel and Schaarschmidt, 1966; Anderson and Anderson, 2003). Suggested reconstructions of structurally similar Jurassic bennettitalean flowers include Williamsoniella coronata (Harris, 1969: p. 143, text-fig. 61A) and Amarjolia dactylota (Bose) Bose et al. (Bose et al., 1984). We are not aware of any Triassic bennettitalean reproductive organ that closely resembles the Lunz flower. 4.4. Systematic position The presence of a robust perianth and the attachment scars of the ovulate structure and pollen organs strongly suggest that the affinities of the reassembled flower from Lunz lie with the Williamsoniaceae. Members of this family are characterised by unisexual or bisexual flowers that were apparently fully exposed and had a resistant perianth, which may have functioned in protection of the reproductive organs within the developing bud. Williamsoniaceous flowers are composed of bract-covered shoots that are borne intercalated among leaf bases, and terminal ovulate cones with surrounding pollen organs and bracts (Sahni, 1932; Harris, 1969; Stewart and Rothwell, 1993; Taylor et al., 2009: p. 732 ff.). In contrast, cycadeoidaceous flowers are borne on short pedicels in the axils of leaves (cataphylls), and are deeply sunken in the ramentum covering the stem (Wieland, 1916; Delevoryas, 1963; Crepet, 1972; Delevoryas, 1975; Crane, 1985; Taylor et al, 2009: p. 728 ff.). It has been suggested that they did not at any stage of development arise above the surface of the ramentum and that they never opened fully (Delevoryas, 1968; Crepet, 1974). The central ovulate cone is surrounded by pinnate pollen organs that are fused proximally. The pollen organs in turn are surrounded by a number of apparently delicate bracts (cf. e.g., Delevoryas, 1968). It is commonly accepted that Cycadeoidaceae are the younger family (Taylor et al., 2009: p. 724, 732); however, the temporal range of Williamsoniaceae did not end with the appearance of the Cycadeoidaceae (e.g., Watson and Sincock, 1992). Additional indications with regard to the affinities of the Lunz flower in the Williamsoniaceae include the slender shape of the associated sterile leaves, which are characteristic of members in that family. Indirect evidence includes the absence of massive, squat bennettitalean trunks in the Lunz flora. The only bennettitalean stem fossil that has been described from the Alpine Triassic is a slender williamsonaceous trunk of a “Pterophyllum plant” from the flora from Neuewelt, Switzerland, which is also Carnian in age and structurally similar to Lunz (Kräusel and Schaarschmidt, 1966). A phylogenetic analysis focusing on the relationships among the Bennettitales (Crane, 1988) resolves the equivocal Triassic Bennettitales as the earliest branching lineages, followed by undisputed members of the Williamsoniaceae and finally members of the Cycadeoidaceae. Although new material and refined analyses of the bennettitalean reproductive organs have been produced since this analysis was published, and some of the bennettitalean reproductive organs from Lunz are today known to have been misinterpreted by earlier workers, the general pattern of character evolution suggested by Crane (1988) is to a large extent supported by our observations. The morphology of Haitingeria krasseri suggests that early bennettitalean flowers had small pollen organs with spreading and well-exposed

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pollen sacs. Larger pollen organs with pollen sacs positioned on the inner surface of inwardly curved pollen organs characterise geologically younger forms (see restorations in Harris, 1969; Bose et al., 1984; Crane, 1985; Watson and Sincock, 1992). The individual pollen organs were entirely free in H. krasseri, while Jurassic and Cretaceous Bennettitales usually have pollen organs that are fused laterally to form a more or less pronounced cup as seen in species of Weltrichia (cf. e.g., Schuster, 1911; Delevoryas, 1991; Watson and Sincock, 1992). Another plesiomorphic feature of H. krasseri is the simple, free pollen sacs. Pollen sacs are also free in the Liassic Weltrichia mirabilis contrasting the synangiate organisation of the pollen-producing units in Middle–Late Jurassic and Cretaceous Bennettitales (Harris, 1969; Crane, 1988). Other possible plesiomorphic features of the Lunz flower include the low number of seeds, relatively large seed size, and high number of interseminal scales in relation to ovules/seeds. Approximately 25– 30 seeds occur in Bennetticarpus wettsteinii, whereas there are up to several hundred ovules/seeds in most Jurassic and Cretaceous ovulate organs (Harris, 1969; Sharma, 1976; Crane, 1988; Watson and Sincock, 1992). The seeds of the Lunz flower are up to 13 mm long and have a rather distinct, probably fleshy outer layer. Low ovule/seed numbers and large seeds also characterise Vardekloeftia, another early bennettitalean plant from the Upper Triassic of Greenland (Harris, 1932; Pedersen et al., 1989). However, interpreting low seed numbers and high number of interseminal scales as ancestral states in the Bennettitales conflicts with the suggestion that interseminal scales represent aborted ovules (e.g., Crane, 1988) and favour the hypothesis that bennettitalean ovulate structures represent strongly modified remnants of a compound branched ovulate structure with interseminal scales representing bracts rather than aborted ovules. 4.5. Reproductive biology The pollination biology of bennettitaleans remains incompletely understood. Beetles are believed to have become increasingly important as pollinators for several groups of bennettitaleans during the Mesozoic (Crowson, 1981; Lawrence and Newton, 1982). The earliest representatives of the modern beetles appeared in the early Late Triassic, and already by the middle and late Late Triassic the group was diverse and abundant (cf. Grimaldi and Engel, 2005; Labandeira, 2006). This early evolutionary diversification of modern beetles, especially reticulated beetles (Cupedidae), apparently occurred parallel to the early evolution of Bennettitales, and hence it is possible that a closer co-evolutionary relationship existed between beetles and Bennettitales (Sitte et al., 1998; Grimaldi and Engel, 2005). In cycads, most of the modern, nonanemophilic forms are pollinated by beetles (Norstog and Nicholls, 1997). Cycads are believed to be not closely related to bennettitaleans, but show analogies in gross morphology and leaf architecture. It is interesting to note that insect eggs perhaps produced by members of the Cupedidae have been found on another Nilssoniopteris species from Lunz [i.e. N. haidingeri (Stur ex Krasser) Pott et al.]. This may suggest that some kind of plant–insect interaction was established between beetles and bennettitaleans in the Lunz ecosystem (Pott et al., 2008b). Whether this interaction also included pollination remains uncertain. The open and pinnate architecture of the pollen organs (Haitingeria krasseri) rather suggest wind-pollination. The larger seed size of Late Triassic Bennettitales (such as Bennetticarpus wettsteinii and species of Vardekloeftia) compared to the smaller seeds of Jurassic and Cretaceous Bennettitales could be evolutionary determined with larger seeds being the ancestral state within the group. Alternatively, seed size may also have been affected by ecological parameters. For example, extant plants that produce large and fleshy seeds are often found in dense vegetation (Kstrategy), while small seeds characterise plants that thrive in open habitats (r-strategy) (Eriksson et al., 2000). Humid conditions, which generally favour dense vegetation, have been inferred for both the

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Lunz flora (Pott et al., 2008a) and the Rhaetian floras of Scania and East Greenland (Norling et al., 1993), while dry, open conditions have been suggested for many Jurassic and Cretaceous floras containing bennettitaleans with small seeds (e.g., Bose and Kasat, 1970; Watson and Sincock, 1992). This picture is, however, not straight forward, since other Jurassic bennettitaleans that produced small seeds (as those from the Yorkshire flora) are believed to have grown under more humid and seasonal conditions in a deltaic environment (Harris, 1969; Van Konijnenburg-van Cittert and Morgans, 1999). The fruit-like, carnose appearance and coherent outer layer of the mature Bennetticarpus wettsteinii seed cones, together with the weakly cutinised seeds, indicate that the cones were abscised as single dispersal units (Harris, 1973). This mode of abscission is more frequently found in plants growing in dense vegetation where larger fruiting units have a better chance to attract frugivorous animals than small isolated seeds (e.g., Norstog and Nicholls, 1997). Moreover, large seeds have a better chance to pass undamaged through the digestive system of an animal. Smaller seeds, which generally are better adapted to be released and dispersed individually, are suggestive of wind dispersal, rather than animal dispersal. As a result, wind dispersal has been proposed for some of the younger Bennettitales by Sharma (1976). General observations reveal that the proportion of winddispersed species typically increases with increasing openness/ dryness of the habitats (Howe and Smallwood, 1982) and, vice versa, animal-dispersed species are often more abundant in dense vegetation. Seed-dispersing animals, in return, facilitate the development of denser or close vegetation (e.g., Eriksson et al., 2000). 5. Conclusions The Bennettitales occupy a key position in many phylogenetic discussions on angiosperm origin and relationships among seed plants. Determining ancestral features for the Bennettitales therefore is of great importance, but to a large extent impeded by the meagre record from the earliest phases of bennettitalean diversification. As a result, a complete bennettitalean flower from the Upper Triassic of Lunz is of particular interest. The flower detailed in this study is reconstructed from several isolated parts based on correspondences in morphological features, but, more important, on similarities in epidermal characters studied from the well-preserved cuticles. The reconstruction supports previous suggestions that early bennettitaleans had large seeds and a much lower number of seeds than later forms, as well as separate, non-fused pollen organs with pollen sacs that are not organised into synangia. However, our interpretation of the fossils as a bisexual flower questions the generally accepted view that early bennettitaleans generally had unisexual flowers. While it cannot be ruled out that the organs belonged to male and female flowers instead of bisexual flowers, there is stronger evidence in support of a bisexual nature of the flower. As a result, the reconstruction of a Late Triassic bennettitalean flower may ultimately assist in framing the broader discussion about the phylogenetic position and relationships of the Bennettitales. Since the reconstruction remains tentative, we refrain from formally proposing a name at this time. Acknowledgements Financial support for this study was provided by the Deutsche Forschungsgemeinschaft (DFG grant KR 2125/3-1 and KR 2125/3-2 to M. K. and H. K.). We are grateful to I. Draxler, I. Zorn and B. Meller (Vienna, Austria), M. Harzhauser and A. Kroh (Vienna, Austria), T. Denk (Stockholm, Sweden), M. Groß (Graz, Austria), H. Steininger (St. Pölten, Austria) and V. Wilde (Frankfurt am Main, Germany) for making the Lunz material for study available. Special thanks are due to Polyanna van Knorring (Stockholm, Sweden) for drawing Figs. 2 and 3. We also thank Johanna H. A. van Konijnenburg-van Cittert (Leiden, the Netherlands),

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