Modified Basal Elements in Dicroidium Fronds (Corystospermales)

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Modified basal elements in Dicroidium fronds (Corystospermales)

ARTICLE in REVIEW OF PALAEOBOTANY AND PALYNOLOGY · DECEMBER 2012 Impact Factor: 1.94 · DOI: 10.1016/j.revpalbo.2011.10.012

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Ignacio H Escapa Edith Taylor Museo Paleontológico Egidio Feruglio University of Kansas

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Research papers Modiﬁed basal elements in Dicroidium fronds (Corystospermales)

Benjamin Bomﬂeur a,⁎, Ignacio H. Escapa b, Edith L. Taylor a, Thomas N. Taylor a a Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence, KS 66045-7600, USA b CONICET, Museo Paleontológico Egidio Feruglio, Av. Fontana 140, Trelew, Chubut 9100, Argentina article info abstract

Article history: We describe a distinct type of heteromorphic basal frond element in four species of the seed-fern foliage Received 12 August 2011 Dicroidium, based principally on a survey of plant-fossil collections from the Triassic of Antarctica. The mod- Received in revised form 28 October 2011 ified foliar elements are conspicuously enlarged, and arise at wide angles and obliquely to the frond plane. Accepted 31 October 2011 Those of D. elongatum and D. crassinerve arise more or less directly from the petiole base; they are overall Available online 6 November 2011 wedge- to fan-shaped with variably dissected margins and fan-shaped venation. Those of D. odontopteroides and D. dubium are (sub)circular, reniform, or obcordate, also with fan-shaped venation, or divided into nar- Keywords: cyclopterid row tongue-shaped segments with alethopteroid venation. The basal elements of some species commonly aphlebia occur isolated. By analogy with comparable structures among other plant groups, we conclude that the stipule basal elements represent a distinct, early leaf-ontogenetic architectural unit in the frond bauplan of Dicroi- taxonomy dium, which provides an important additional character for a more accurate delimitation and systematic clas- palaeoecology sification. Similar structures also occur on the corystosperm reproductive organs Umkomasia and Pteruchus.It seed ferns appears that the basal elements were particularly common among high-latitude Dicroidium trees that flour- ished in a strongly seasonal light regime. We hypothesize that the modified elements may represent the initial foliar outgrowths during spring flush, ensuring a rapid re-initiation of sap flow and metabolic activity after the extended period of winter dormancy. © 2011 Published by Elsevier B.V.

1. Introduction et al., 2007; Morel et al., 2010), there is increasing evidence that these foliage types should more appropriately be included in a single, Detailed documentation of leaf architecture contributes to a better more naturally defined genus, Dicroidium Gothan emend. Townrow understanding of the biology and ecology of seed ferns, and can also (e.g., Townrow, 1957; Bonetti, 1966; Archangelsky, 1968; Anderson provide significant characters for systematic classification (e.g., and Anderson, 1983; Holmes and Anderson, 2005; Bomfleur and Laveine, 1967, 1997; Laveine et al., 1993; Krings et al., 2001, 2006). Kerp, 2010). Compared to Palaeozoic foliage taxa, however, few studies have The concept of Dicroidium as a biological entity has been greatly addressed details of leaf architecture among Mesozoic seed ferns advanced, especially in recent decades. In their work on the Triassic (e.g., Rees and Cleal, 1993). A prominent type of Mesozoic seed-fern Molteno Formation of South Africa, Anderson and Anderson (1983) foliage consists of the characteristically bifurcate fronds of the Corys- have provided a comprehensively illustrated documentation of the tospermales from the Triassic of Gondwana. The foliage shows wide natural variability of Dicroidium fronds sensu lato. Of particular im- morphological variability and plasticity, which renders taxonomic de- portance are several specimens that Anderson and Anderson (1983) limitation somewhat problematic (e.g., Townrow, 1957; term hybrid fronds—ones that bear different types of pinnules that Archangelsky, 1968; Retallack, 1977; Baldoni, 1980; Petriella, 1981; would be assigned by some authors to separate genera when found Anderson and Anderson, 1983; Boucher et al., 1993; Holmes and detached (see, e.g., Anderson and Anderson, 1983: pl. 74, Fig. 7). Anderson, 2005). As a consequence, no uniform concept for the clas- The anatomy of Dicroidium fronds has also been described based on sification of these fronds has emerged since they were first identified structurally preserved material from the Middle Triassic of the central almost a hundred years ago (Gothan, 1912). Whereas some authors Transantarctic Mountains (Pigg, 1990). The common occurrence of a continue to distinguish among a varying number of separate genera, particular type of secretory cavity has made it possible to affiliate including Dicroidium Gothan, Xylopteris Frenguelli, Johnstonia these permineralized fronds with anatomically preserved pollen or- Walkom, and Zuberia Frenguelli (e.g., Frenguelli, 1943; Retallack, gans, ovulate organs, and stems with attached leaf bases from the 1977; Gnaedinger and Herbst, 1998; Spalletti et al., 2005; Artabe same site (Meyer-Berthaud et al., 1992, 1993; Yao et al., 1995; Klavins et al., 2002). In addition, it has been demonstrated that Dicroidium fronds have a distinctive epidermal anatomy and cuticle morphology, ‘ ’ ⁎ Corresponding author. Tel.: +1 785 864 4255; fax: +1 785 864 5860. including amphistomatic fronds with pseudosyndetocheilic stomata E-mail address: bomfl[email protected] (B. Bomfleur). (sensu Retallack, 1977), which is especially helpful in genus and species

0034-6667/$ – see front matter © 2011 Published by Elsevier B.V. doi:10.1016/j.revpalbo.2011.10.012 16 B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26 identification (Gothan, 1912; Townrow, 1957; Archangelsky, 1968; 3. Results Retallack, 1977; Bomfleur and Kerp, 2010). Such anatomical details, however, can only be studied when the specimens are sufficiently 3.1. Modified basal elements in Dicroidium elongatum (Carruthers) well preserved. Traditionally, it has been thought that Dicroidium was Archangelsky (Plate I; Fig. 1A–C) restricted to the Triassic of Gondwana (Gothan, 1912); however, the recent descriptions of well-preserved Dicroidium fronds from the Permian Localities. (1) Schroeder Hill (85°23′S; 175°12′W) in the Cumulus palaeotropics (Kerp et al., 2006; Abu Hamad et al., 2008)demonstrate Hills, central Transantarctic Mountains, East Antarctica; (2) Mount that a diagnostic concept of Dicroidium as a biological entity should Wisting (86°27′S; 165°26′W), Queen Maud Mountains, central Trans- not include the stratigraphic and palaeogeographic occurrences of the antarctic Mountains, East Antarctica; (3) undetermined locality in the fossils. As a result, it becomes increasingly difficult to maintain a suit- Brisbane area, Queensland, Australia. able taxonomic delimitation of this taxon on one hand and a natural Stratigraphy and age. (1 and 2) Falla Formation (Victoria Group, classification approach on the other. Beacon Supergroup), Late Triassic; (3) Tingalpa Formation (Ipswich Heteromorphic basal pinnules have been reported to occur spo- Coal Measures), early Late Triassic. radically in Dicroidium fronds from South Africa (Townrow, 1962; Material. (1) Twenty-eight individual plant fossils on fifteen spec- Anderson and Anderson, 1983) and Australia (Holmes, 1982), but imens: T1672, 1676, 1678, 1679, 1681, 1690, 1697, 1699, 1706, 1711, this feature has not been studied in detail. Here we describe a distinct 1726, 1731, 1734–1736; (2) one specimen: T1886; (3) one specimen: type of foliar dimorphism among several Dicroidium species, based T6382. mainly on a survey of compression assemblages from several Triassic Description. Fronds are generally 15–20 cm long, bifurcated in the sites in the Transantarctic Mountains. This report provides details lower third at an acute angle, pinnate, and characterized by only a that can contribute to a more robust systematic classification of few distantly spaced, long needle-like and single-veined pinnules, Dicroidium based on biological criteria, and offers a further step in each arising at an acute angle (Plate I, 1, 2). better defining and understanding the physiology and growth strate- Heteromorphic basal elements occur in the form of one opposite gy of the Southern Hemisphere Corystospermales. pair of 1–2 cm long foliar appendages that arise either directly or at a distance of up to ~5 mm from the swollen petiole base (Plate I, 1–5, 10; Fig. 1A–C); they are inserted at angles between 25° and 70° 2. Material and methods and in most cases appear to be inclined or slightly curved basiscopically and obliquely to the frond plane (Plate I,1–5, 10; Fig. 1A–C). This study is based on a survey of collections of Dicroidium assem- The basal elements have a variable morphology ranging from ob- blages from Antarctica housed in the Paleobotanical Collections at the ovate, deltoid, or wedge- to fan-shaped with entire, crenulate, or University of Kansas (PBKU), Lawrence, Kansas, U.S.A. Over the course cleft distal margins (Plate I,2–10); some specimens are deeply dis- of several decades of repeated collecting in Antarctica, multiple sected, forming a cluster of irregular needle-like segments that radi- Dicroidium assemblages were sampled to varying degrees from sever- ate from a small portion of a basal lamina (Plate I, 1, 11). Many of al sites in the Transantarctic Mountains. The collections with hetero- the larger, entire-margined to cleft specimens appear to be slightly morphic Dicroidium fronds described in this study are from Schroeder concave adaxially, forming a sheathing morphology in the basal lam- Hill, the ‘Alfie's Elbow’ site, Mount Falla, and Mount Wisting in the ina portion (Plate I, 2, 3, 5, 8). The venation is fan-shaped and more or central Transantarctic Mountains (all from the Falla Formation, less evenly dichotomizing with usually one vein per ultimate lobule Upper Triassic) and from the Allan Hills and Shapeless Mountain in or segment (Plate I,3–8, 11). southern Victoria Land (Lashly Formation, Middle to Upper Triassic). Remarks. Whereas similar bifurcated fronds with elongate needle- In addition, the Paleobotanical Collections house a single hand speci- like pinnules have been assigned to a separate morphogenus, Xylop- men of a Dicroidium frond with heteromorphic basal elements from teris Frenguelli, by some authors (e.g., Frenguelli, 1943; Retallack, the Carnian (early Late Triassic) Tingalpa Formation of the Brisbane 1977; Gnaedinger and Herbst, 1998; Artabe et al., 2007; Morel et al., area in southeastern Queensland, Australia. 2010), we prefer the approach of Archangelsky (1968; also Other collections of Antarctic Dicroidium assemblages from Gordon Anderson and Anderson, 1983) that includes fronds of this type in Valley and the Marshall Mountains, also in the central Transantarctic Dicroidium. Anderson and Anderson (1983) further distinguish a vari- Mountains (Fremouw or Falla Formations, Middle or Upper Triassic) ety of different forms and subspecies. Dicroidium fronds from the Tri- were surveyed, but did not contain fronds with heteromorphic basal el- assic Molteno Formation of South Africa that are morphologically ements. Species in those assemblages include D. odontopteroides (Mor- similar to the Antarctic material have been described as a distinct ris) Gothan, D. elongatum (Carruthers) Archangelsky, D. dubium subspecies, D. elongatum subsp. dimorphum Anderson et Anderson (Feistmantel) Gothan, D. crassinerve (Geinitz) Anderson et Anderson, (Anderson and Anderson, 1983). Moreover, the specimens from the D. dutoitii Townrow, and D. zuberi (Szajnocha) Archangelsky (see, e.g., central Transantarctic Mountains resemble D. elongatum subsp. mata- Escapa et al., 2011). tifolium Anderson et Anderson and D. elongatum subsp. argentinum

Plate I. Modiﬁed basal elements in Dicroidium elongatum (Carruthers) Archangelsky from (1–3, 5–11) the Upper Triassic Falla Formation at Schroeder Hill (Cumulus Hills, central Transantarctic Mountains) and (4) the Upper Triassic Tingalpa Formation of the Brisbane area, Queensland, Australia.

1. Almost intact frond with a pair of modified basal elements that are highly dissected into radiating linear segments (lower arrow). Note that the right-hand frond segment above the bifurcation (upper arrow) has broken off almost entirely towards the center right of the image. T1726b. 2. Fragmented frond with deltoid basal elements with adaxially concave lamina. T1734b. 3. Detail of the counterpart specimen of Fig. 1B. T1734a. 4. Wedge-shaped basal element with rounded, crenulated distal margin and fan-shaped, dichotomizing venation. T6382. 5. Frond base with two fan-shaped basal segments showing concave laminae and fan-shaped venation. T1682. 6. Isolated obovate basal element with fan-shaped, dichotomizing venation. T1672. 7. Wedge-shaped basal element with incised distal margin. T1682. 8. Isolated wedge-shaped basal element with variably dissected distal margin. T1735. 9. Three deltoid to fan-shaped basal elements. T1681b. 10. Frond base with attached pair of wedge-shaped basal elements. T1697. 11. Detail of the counterpart specimen of Plate I, 1, showing deeply dissected basal elements forming irregular clusters of radiating, needle-like segments. T1726a. Scale bars=1 cm (1, 2, 11), 5 mm (3–10). B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26 17 18 B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26

Fig. 1. Schematic drawings highlighting morphology and venation of modiﬁed basal foliar elements of Dicroidium Gothan fronds from the Middle–Upper Triassic of Antarctica and Australia. A, Dicroidium elongatum (Carruthers) Archangelsky. T1734b (see Plate I, 2). B, Dicroidium elongatum. T1679 (see Plate I, 10). C, Dicroidium elongatum. T6382 (see Plate I, 4). D, E, Dicroidium crassinerve (Geinitz) Anderson et Anderson. T1899 (see Plate II,1–3). F, Dicroidium odontopteroides (Morris) Gothan. T1474 (see Plate II, 6). G, Dicroidium odontopteroides. T1178 (see Plate II, 5). H, Dicroidium sp. cf. D. odontopteroides. T1520 (see Plate II, 9). I, Dicroidium sp. cf. dubium. T128 (see Plate III, 3).

(Kurtz) Anderson et Anderson (=Xylopteris argentina (Kurtz) Fren- venation (Plate II, 2, 3). In one specimen, the attached basal element guelli), which are both characterized by having very few and distantly appears as a distinct outgrowth of the petiole base and runs parallel spaced pinnules (Anderson and Anderson, 1983). to and is more or less sheathing the actual petiole in its basal portion; Occurrence. In the Schroeder Hill assemblage, each preserved basal the second element is detached, but only slightly displaced from the frond portion of D. elongatum contains modified foliar elements. The petiole base (Plate II, 2). In the second specimen, the preserved sample from the Tingalpa Formation consists of a single preserved basal element arises immediately above the petiole base and is frond base with attached basal foliar elements. In addition, isolated abruptly inclined basiscopically at an angle of about 100° to the peti- basal elements commonly occur at Schroeder Hill and on one slab ole; the lamina portion arises obliquely to the frond plane (Plate II, 3). from Mount Wisting. Remarks. Based on the widely spaced pinnules and the distally crenulate and basally decurrent pinnule margins, these fossils agree 3.2. Modified basal elements in Dicroidium crassinerve (Geinitz) Ander- most closely with Dicroidium crassinerve forma stelznerianum (Gei- son et Anderson (Plate II, 1–3) nitz) Anderson et Anderson and D. crassinerve forma trilobitum (John- ston) Anderson et Anderson (Anderson and Anderson, 1983). Locality. Mount Wisting (86°27′S; 165°26′W), Queen Maud Moun- Occurrence. The collection from Mount Wisting contains two spec- tains, central Transantarctic Mountains, East Antarctica. imens with (partially) preserved frond bases, both bearing hetero- Stratigraphy and age. Falla Formation (Victoria Group, Beacon Su- morphic basal elements. In one specimen, one of the basal elements pergroup), Late Triassic. is detached, but only slightly displaced from the petiole base. Material. Two plant fossils on one specimen: T1899. Description. Fronds are pinnate, bifurcated at acute angles in the lower half, and estimated to be up to ~20 cm long (Plate II, 1). Regular 3.3. Modified basal elements in Dicroidium odontopteroides (Morris) pinnae are elongate tongue-shaped to narrow subtriangular, and typ- Gothan (Plate II, 4–9) ically have a lobulate distal margin and a decurrent basiscopic margin; pinnae are generally widely spaced and attached at acute Localities. (1) Unnamed ridge near Schroeder Hill informally called angles (Plate II, 1). ‘Alfie's Elbow’ (84°22′S; 164°55′W), Cumulus Hills, central Transan- Heteromorphic elements arise directly from the swollen petiole tarctic Mountains; (2) undetermined locality in the Allan Hills base (Plate II, 1, 2). They consist of presumably one pair of enlarged (around 76°43′S; 159°40′E), southern Victoria Land, East Antarctica; wedge- or fan-shaped laminar segments with variably crenulate and (3) Shapeless Mountain (77°26′S; 160°24′E), southern Victoria cleft distal margins and fan-shaped, evenly spreading dichotomizing Land, East Antarctica.

Plate II. Modiﬁed basal foliar elements of different Dicroidium Gothan fronds from the Triassic of East Antarctica.

1–3. Dicroidium crassinerve (Geinitz) Anderson et Anderson from the Upper Triassic Falla Formation at Mount Wisting (Queen Maud Mountains, central Transantarctic Mountains). T1899. 1. Almost complete frond with prominently enlarged, fan-shaped basal element attached to the petiole base (arrow). 2. Detail of Plate II, 1, showing attached basal element on the right and detached second element slightly displaced towards the lower left corner of the image. 3. Frond base with a deltoid basal element. 4–6. Dicroidium odontopteroides (Morris) Gothan from the Upper Triassic Falla Formation at the Alfie's Elbow site (Cumulus Hills, central Transantarctic Mountains). 4. Nearly complete frond with a pair of modified basal elements. T1462b. 5. Basal frond portion with a pair of modified basal elements. T1178. 6. Basal frond portion with opposite pair of obliquely attached, obcordate basal elements. Note the fan-shaped venation pattern. T1474b. 7–9. Dicroidium sp. cf. D. odontopteroides from the Middle–Upper Triassic Lashly Formation at Shapeless Mountain (south Victoria Land). 7. Complete frond with fragments of modified basal elements(arrows) T1627a. 8. Detail of Plate II, 7. 9. Detail of a basal frond part with conspicuously enlarged, wedge-shaped basal element divided into narrow-triangular segments with alethopteroid venation. T1520. Scale bars=2 cm (1, 7), 1 cm (4, 8, 9), 5 mm (2, 3, 5, 6). B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26 19 20 B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26

Stratigraphy and age. (1) Falla Formation (Victoria Group, Beacon basal frond portions are preserved, both of which bear remains of a pair Supergroup), Late Triassic; (2) Level 2 in Member C of the Lashly For- of modified basal elements. mation (Victoria Group, Beacon Supergroup), Late Triassic; (3) undetermined position within the Lashly Formation (Victoria Group, 3.4. Modified basal elements in Dicroidium dubium (Morris) Gothan Beacon Supergroup), Middle–Late Triassic. (Plate III, 1–3) Material. (1) Forty-six individual plant fossils on thirty specimens: T 1028, 1038, 1048, 1054, 1105, 1106, 1152, 1155, 1178, 1181, 1184, Locality. (1) Unnamed ridge near Schroeder Hill informally called 1220, 1222, 1231, 1247, 1266, 1267, 1290, 1297, 1299, 1300, 1343, ‘Alfie's Elbow’ (84°22′S; 164°55′W), Cumulus Hills, central Transan- 1347, 1418, 1420, 1464, 1469, 1474, 1482, 1518; (2) two specimens: tarctic Mountains; (2) Mount Falla (84°22′S; 164°55′E), Queen Alex- T 774, 796; (3) two specimens: T1520, 1627. andra Range, central Transantarctic Mountains. Description. The fronds are bifurcated in the lower third to lower Stratigraphy and age. (1 and 2) Falla Formation (Victoria Group, half, pinnate, and about 15 cm, rarely up to 25 cm long. Pinnae are Beacon Supergroup), Late Triassic. closely spaced but separate, orbicular, rounded subrhombic to Material. (1) Four specimens: T992, 1040, 1115, 1518; (2) one tongue-shaped. Venation is generally odontopteroid, but may attain specimen: T128. alethopteroid morphology with a more-or-less pronounced midvein Description. Fronds are comparatively large (up to ~25 cm long), in more elongated pinnules (Plate II,4–9). bifurcated in the lower half, and bipinnatifid; pinna morphology Heteromorphic basal elements are generally attached at about ranges from simple and elongate tongue-shaped to pinnately lobed 5–10 mm above the frond base and closer to the superpositioned pin- to partially pinnulate (Plate III, 1). The largest pinnae and the greatest nule pair (e.g., Plate II, 4), but may also arise immediately above the complexity generally occur in the central part of the frond, giving the petiole base; they are conspicuously larger than the superpositioned blades above the bifurcation a broadly elliptic to lanceolate outline. pinnules and attached at wider angles (in some cases >90°) (Plate The venation is alethopteroid, with odontopteroid vein groups in II,4–9). pinna lobes and pinnules (Plate III, 1). In the fossils from the Alfie's Elbow site and Allan Hills, hetero- Heteromorphic basal elements occur in the form of an opposite morphic elements consist of one opposite pair of ovate-(sub)circular pair of primarily two-lobed laminar outgrowths that arise at almost to broadly reniform foliar elements that may have a shallow distal right angles from the petiole (Plate III, 2, 3). The lobes range from sinus or indentation, appearing more or less obcordate (Plate II, shallowly divided, broadly tongue-shaped, and rounded, resulting in 4–6). If well preserved, the basal elements appear to be attached a slightly asymmetrical obcordate shape (Plate III, 2), to deeply divid- obliquely to the plane of the frond, with the basiscopic margins over- ed, strongly elongated, and narrowly tongue-shaped, with each seg- lapping the petiole and the acroscopic margins being partially cov- ment bearing a small lateral secondary lobe (Plate III, 3). The ered by the superpositioned pinnules (e.g., Plate II, 5, 6). The venation is fan-shaped and evenly spreading into the lobes in the ob- venation is fan-shaped and evenly spreading into the lamina or lam- cordate elements to alethopteroid with a pronounced midvein in ina lobes (Plate II, 6). more elongated segments (Plate III, 2, 3). In the fossils from Shapeless Mountain, only fragments of the pairs Remarks. The specimens from Alfie's Elbow can be readily placed of modified basal elements are preserved. In one specimen, the more in Dicroidium dubium as described, e.g., by Anderson and Anderson completely preserved basal element has an oblanceolate outline with (1983). The single frond fragment with heteromorphic basal ele- an elongate and asymmetrically tapering central segment and two ments from Mount Falla was already figured and described as D. small lateral lobes (Plate II, 7, 8). In the second specimen, the basal el- dubium by Boucher et al. (1993). There is some evidence, however, ement is broadly wedge-shaped and deeply divided distally into three to suggest that all Dicroidium fronds from the Mount Falla assemblage more-or-less equally developed, triangular segments with acute api- belong to a single species, D. lancifolium (Morris) Gothan (Bomfleur et ces and alethopteroid venation (Plate II, 9). al., 2011). In the context of the present paper, we contend that it is Remarks. Following the classification of Anderson and Anderson best to provisionally describe this particular fragment from Mount (1983), the specimens from Alfie's Elbow site correspond most close- Falla as Dicroidium sp. cf. D. dubium. ly to Dicroidium odontopteroides subsp. odontopteroides (Morris) An- Occurrence. Heteromorphic basal elements occur consistently in derson et Anderson, which is characterized by more elongated the few complete basal frond portions of Dicroidium dubium at the pinnules with well-developed midveins, whereas the material from Alfie's Elbow site; only a single specimen has been recorded in the as- the Allan Hills appears more similar to D. odontopteroides subsp. orbi- semblage from Mount Falla. culoides Anderson et Anderson based on the rather orbicular pinnule shape and strictly odontopteroid venation. 4. Discussion The specimens from Shapeless Mountain are included in Dicroidium odontopteroides only with some reservation, because they differ from 4.1. Comparison of the morphologies and distribution of basal foliar those of the other two localities in being larger, having more deeply elements in Dicroidium lobed basal elements, and bearing consistently tongue-shaped pinnules with constricted basal margins. In general, the specimens are equally Almost all modified basal elements have some general features in similar to D. odontopteroides subsp. odontopteroides and D. crassinerve common: (1) they occur primarily in the form of an opposite or sub- forma crassinerve of Anderson and Anderson (1983). The latter two fea- opposite pair; (2) they are conspicuously enlarged compared to the tures appear to be rather typical of Dicroidium sp. A of Bomfleur superpositioned pinnules of the same frond; (3) they arise from a andKerp(2010), which is mainly distinguished by characteristic epi- narrow point of attachment and at wider angles than the regular pin- dermal and cuticular features that cannot be observed in the present nules; and (4) the lamina is oriented obliquely to the frond plane (see material. Fig. 1). Apart from these overall similarities, the basal elements can be Occurrence. The development of modified basal elements in classified into two major groups that we here informally term type A Dicroidium odontopteroides is variable in the assemblages from Alfie's and type B. Elbow and the Allan Hills. Although many of the complete basal frond Type A basal elements occur in Dicroidium elongatum and D. cras- portions bear enlarged, modified basal elements that differ conspicu- sinerve. Characteristic features include: (1) an attachment either di- ously from the regular pinnules, others lack distinctly modified ele- rectly or at only a short distance from the swollen petiole base; (2) ments and appear to bear a basal pair of small regular pinnules basiscopic curving or inclination; (3) adaxially concave to partly instead. In the assemblage from Shapeless Mountain, only two complete sheathing basal lamina portions; (3) deltoid, wedge-, or fan-shaped B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26 21

Plate III. Modiﬁed basal foliar elements in Dicroidium dubium (Morris) Gothan and Dicroidium sp. cf. D. dubium from the Upper Triassic Falla Formation of the central Transantarctic Mountains.

1. Nearly complete frond from the Alfie's Elbow site (Cumulus Hills, central Transantarctic Mountains). T992b. 2. Detail of Plate III, 1, showing opposite pair of basal elements with two tongue-shaped lobes. 3. Frond base of Dicroidium sp. cf. D. dubium from Mount Falla (Queen Alexandra Range) showing basal element with two elongate tongue-shaped segments and alethopteroid venation. T128. Scale bars=2 cm (1), 1 cm (2), 5 mm (3). outlines with variably crenulate, incised, to deeply dissected margins; limited number of sufficiently complete fronds, it is difficult to esti- and (4) fan-shaped, repeatedly dichotomizing venation (Fig. 1A–E). mate the frequency of modified basal elements in Dicroidium sp. cf. Type A elements appear to be consistently present (or consistently D. odontopteroides from Shapeless Mountain, D. dubium from Alfie's absent) in individual assemblages, and also occur commonly in the Elbow, and Dicroidium sp. cf. D. dubium from Mount Falla. form of isolated elements that are detached from the actual frond. It is remarkable that there are only a few previous reports of mod- Type B basal elements occur in Dicroidium odontopteroides and D. ified basal elements in Dicroidium fronds. In his study of the corystos- dubium. Unlike those of type A, these elements are attached to the perm pollen-organ Pteruchus Thomas emend. Townrow, Townrow petiole mostly at about 5–10 mm above the frond base, and are closer (1962) referred to a modified “[…] basal pinnule sometimes pro- to the superpositioned pinnule pair (e.g., Fig. 1F, G). Morphologies duced by leaves of the Dicroidium–Xylopteris group” (Townrow, range from (sub)circular, reniform, or obcordate in D. dubium and D. 1962, p. 315) to support his assumption that Pteruchus represents a odontopteroides from Alfie's Elbow and the Allan Hills (e.g., Plate III, modified sporophyll instead of a fertile branch system (see discussion 2; Fig. 1F, G) to primarily wedge-shaped and deeply divided with below). The only additional reports that we are aware of are those of narrow-triangular or tongue-shaped segments in Dicroidium sp. cf. (1) Holmes (1982), who noted a pair of modified basal elements on a D. odontopteroides from Shapeless Mountain and Dicroidium sp. cf. D. frond of D. odontopteroides from New South Wales; (2) Anderson and dubium from Mount Falla (Fig. 1H, I). The lamina division shows a Anderson (1983), who described D. elongatum fronds from South Af- tendency to produce two, slightly asymmetrical major lobes or seg- rica with enlarged basal foliar elements that are similar to the present ments (Plate III,2;Fig. 1F, G, L). The venation pattern is fan-shaped, material; and (3) Holmes and Anderson (2005), who figured aber- spreading, and repeatedly dichotomizing in the more robust elements rant, multiply forking fronds of D. odontopteroides each with a pair (Fig. 1F), but may attain alethopteroid morphology in prominently of conspicuously modified foliar elements near the petiole base elongated lamina segments (Fig. 1H, L). In contrast to type A ele- (Holmes and Anderson, 2005, Figs. 5b, c, 6a). On one hand, this scar- ments, type B elements show varying degrees of modification com- city of previous reports is likely due to a strong bias in the preserva- pared to the regular pinnule morphology. This is demonstrated in tion, collection, and identification of these elements. Unlike regular the comparatively large collection of D. odontopteroides from Alfie's Dicroidium pinnules, the basal outgrowths were apparently easily de- Elbow and the Allan Hills, in which basal foliar elements may be tached from the frond (see, e.g., Plate I,6,8;Plate II, 2), which renders more or less conspicuously modified compared to superpositioned the preservation of these elements much more dependent on favor- pinnules, or in other cases, may not be modified at all. Due to the able taphonomic conditions. It also may be that modified frond 22 B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26 elements occur more frequently, but have simply been overlooked or Potonié, 1903; Hirmer, 1927; Phillips and Galtier, 2005). Similar not identified as belonging to Dicroidium. Compared to the frond por- structures were subsequently found on extant cyatheaceaen tree tions above the dichotomy, the frond base is likely to be disregarded ferns (Potonié, 1903; Bower, 1910; Marloth, 1913; Hill, 1932; as in many cases it does not show the fully developed, taxonomically Tardieu-Blot, 1941). Seed-fern cyclopter(o)ids and fern aphlebiae significant pinna morphologies. There may be some evidence for this are regarded by most authors as specialized outgrowths of the actual hypothesis in that many illustrations of Dicroidium fronds in the liter- frond blade, i.e., heteromorphic pinnae or pinnules (Goebel, ature do not include the frond base, even though it may originally 1898–1901; Potonié, 1903; Bower, 1910; Laveine, 1997, 2005; have been preserved. On the other hand, it is also plausible that the Phillips and Galtier, 2005). Descriptions of immature fronds bearing formation of modified basal elements was controlled by particular en- fully developed cyclopter(o)id or aphlebioid elements that entirely vironmental parameters. In this case, the common occurrence of enclose the delicate croziers demonstrate that both of these types of these elements in Antarctic Dicroidium assemblages, which were situ- heteromorphic elements differentiated during early stages of frond ated at comparatively high palaeolatitudes, may reflect pronounced ontogeny (see, e.g., von Roehl, 1868; Stur, 1875; Howse, 1888; seasonality and periodic growth cycles (see Section 4.5). Potonié, 1903; Hirmer, 1927; Laveine, 2005). Functionally and morphologically similar structures occur among 4.2. Structure and developmental state of the basal foliar elements angiosperms in the form of laminar stipules. Unlike the cyclopter(o)ids and aphlebiae of fern and seed–fern fronds, however, stipules are The heteromorphic elements reported here include a similar basic paired outgrowths of the petiole base that are vascularized indepen- morphology among different species and are quite common in some dently from the emerging petiole and leaf blade (Goebel, 1898–1901; of the Antarctic assemblages, even though they may not be consis- Lubbock, 1899; Sinnott and Bailey, 1914; Majumdar, 1956). As such, tently expressed (or preserved) in every frond. We interpret the het- they do not represent modified elements of the blade, i.e., heteromor- eromorphic basal elements as a distinct architectural unit in the basic phic leaflets or pinnules, but rather a modification of the petiole base frond bauplan of Dicroidium. Detailed interpretations regarding the that is independent from the leaf blade. Analogous stipular outgrowths structure and developmental state of the modified basal elements re- also occur in other plant groups, including cycads (Bower, 1910; main difficult at present, mainly because nothing is known about the Stevenson, 1992)andvariousfernfamilies(e.g.,Goebel, 1898–1901; leaf ontogeny of Dicroidium fronds. This is no doubt due to the decid- Bower, 1910). Stipules and stipular outgrowths are in many cases cadu- uous growth habit of the Dicroidium plants (see Meyer-Berthaud et cous, i.e., they are produced at an early leaf-ontogenetic stage and com- al., 1992; Taylor, 1996; Cúneo et al., 2003; Taylor et al., 2006; monly lost during subsequent maturation (e.g., Goebel, 1898–1901; Bomfleur and Kerp, 2010). Deciduousness greatly reduces the oppor- Lubbock, 1899; Gifford and Foster, 1989). Although stipules are initial tunity to find leaves that are preserved in organic attachment to the foliar outgrowths of the petiole base, they may become transposed subtending organs; this growth habit also makes it difficult to obtain onto the petiole itself due to intercalary growth (e.g., Goebel, information on leaf ontogeny and development, as the leaves are in- 1898–1901; Lubbock, 1899). In other cases, aberrant growth may variably shed in a mature state. In order to examine the structure cause the formation of displaced stipules or stipule-like basal leaflets and origin of the basal foliar outgrowths in Dicroidium fronds, it ap- (intermediates of Cook, 1923;seeTattersall et al., 2005; Efroni et al., pears promising to search for common features among morphologi- 2010). cally similar structures in other plant groups. Possible analogs When taken together, the primary developmental feature common considered here include (1) the cyclopter(o)id elements in Palaeozoic to all heteromorphic basal foliar elements among the plant groups con- medullosalean seed ferns, (2) the aphlebiae in fossil and extant ferns, sidered is that they differentiate prior to actual frond or leaf-blade de- and (3) the stipule of angiosperm leaves together with stipular out- velopment. Furthermore, in many cases, they are ephemeral growths in other plant groups. structures that may be shed during subsequent leaf maturation. By Cyclopteris Brongniart and Aphlebia Presl in Sternberg are en- analogy, we hypothesize that the same also applies to the modified larged, entire-margined or variably lobed to dissected leaf-like fossils basal elements in Dicroidium. This is supported by the fact that the known from the Carboniferous of Europe as early as the first half of basal elements commonly occur detached from the actual frond (see the 19th century (e.g., Brongniart, 1828; Sternberg, 1833). These foli- Plate I,6,8;Plate II,2;Anderson and Anderson, 1983, pl. 54: Figs. 24, ar structures were recognized early as heteromorphic basal elements 25, 28–33, pl. 75: Fig. 7), whereas, by comparison, regular pinnules of fern-like fronds (Lindley and Hutton, 1833; von Roehl, 1868; Florin, are rarely ever found isolated. Moreover, there is some evidence to sug- 1925). Cyclopterids are typically orbicular elements with spreading gest that at least the type A elements of D. elongatum and D. crassinerve venation that were produced on fronds of the late Palaeozoic Medul- represent stipular outgrowths, as they originate in many cases directly losales (Pteridospermophyta); they were originally attached on basal from the swollen petiole base (see, e.g., Plate I,3,10;Plate II,2; petiole and rachis portions, and are commonly found isolated (e.g., Fig. 1A, D, E). The peculiar heteromorphic element on Dicroidium sp. Florin, 1925; Crookall, 1959; Laveine, 2005; Lyons and Laveine, cf. D. dubium from Mount Falla is borne on a short stalk that, although 2005). True Cyclopteris elements, characterized by an orbicular out- positioned at some distance from the base, appears to arise from the line and entire margins, occur on fronds of Laveineopteris Cleal et al. base rather than from the petiole itself (Plate III,3;Fig. 1L). Finally, (e.g., Cleal and Shute, 2003; Laveine, 2005) and Neuropteris Brong- the interpretation of these elements as independently vascularized stip- niart sensu stricto (e.g., Beeler, 1983; Lyons and Laveine, 2005). ular outgrowths may be further supported by the nodal topography of Closely comparable foliar elements with entire or dissected margins, the stems of the corystosperms, Rhexoxylon Bancroft emend. Archan- so-called cyclopteroid elements, however, are also known to occur gelsky et Brett and Kykloxylon Meyer-Berthaud, Taylor et Taylor, on other medullosan fronds, including Odontopteris Brongniart, Les- which both produce multiple ‘gaps’ in the xylem cylinder at the point curopteris Schimper, Callipteridium Weiss, Margaritopteris Gothan, of each leaf trace emission (Archangelsky and Brett, 1961; Meyer- and Blanzyopteris Krings et Kerp (see, e.g., Laveine, 1997, 2005; Berthaud et al., 1992, 1993). Among angiosperms, there is a strong cor- Krings and Kerp, 1999; Krings et al., 2006). This latter genus is of par- relation between nodal topography and formation of stipules, which ticular interest, as it represents the only other frond bearing just a sin- occur almost exclusively in families with more than a single ‘gap’ per gle, opposite basal pair of modified elements like the plant fossils leaf trace (Sinnott and Bailey, 1914). described here (Krings and Kerp, 1999). Thus, we interpret the basal foliar outgrowths on Dicroidium Aphlebiae are sheathing, variably dissected modified foliar ele- fronds as a distinct, possibly caducous developmental unit that differ- ments on fern axes and petioles, and were first described from entiated during early stages of leaf development and was commonly Palaeozoic ferns (e.g., Lindley and Hutton, 1833; Sternberg, 1833; shed during further growth and maturation of the frond. B. Bomfleur et al. / Review of Palaeobotany and Palynology 170 (2012) 15–26 23

Fig. 2. Idealized reconstructions of different Dicroidium fronds with modiﬁed basal foliar elements. A, B, Dicroidium elongatum (Carruthers) Archangelsky. C, Dicroidium crassinerve (Geinitz) Anderson et Anderson. D, Dicroidium odontopteroides (Morris) Gothan. E, Dicroidium sp. cf. D. odontopteroides.

4.3. Taxonomic and systematic implications 4.4. Phylogenetic considerations

Although the genus Dicroidium was established almost a hundred The peculiar morphology of the basal elements provides an oppor- years ago (Gothan, 1912) and identified as the characteristic foliage tunity to speculate about the underlying leaf-architectural model and of the Gondwanan corystospermalean seed ferns soon thereafter its possible phylogenetic significance. In this regard, the tendency to (Thomas, 1933), the systematic treatment of these fronds still remains produce two main lobes or segments is a particularly interesting fea- problematic (e.g., Baldoni, 1980; Anderson and Anderson, 1983; ture of the Type B elements. It is tempting to interpret this bi-lobed to Boucher et al., 1993; Holmes and Anderson, 2005). In this context bifurcate morphology as a replication of the main dichotomy in the the presence of modified basal foliar elements represents an impor- frond bauplan of Dicroidium. In fact, the large bifurcate element at- tant additional taxonomic character that contributes to a more accu- tached to the base of a Dicroidium sp. cf. D. dubium frond from rate circumscription of the genus. Apart from the cyclopter(o)ids of Mount Falla (Plate III, 3) is somewhat reminiscent of small fronds of the late Palaeozoic Medullosales, we are unaware of comparable entire-margined Dicroidium species, such as D. dutoitii or D. coriaceum frond elements in any other seed–fern group. (see, e.g., Anderson and Anderson, 1983, pl. 76: Figs. 4, 5, 12, 13, 17, In a practical sense, the occurrence of modified basal elements 27; Holmes and Anderson, 2005, Fig. 2a–c). may be especially helpful for discrimination at higher taxonomic However, there may also be some evidence for a throwback to an- ranks. For example, in cases where basal elements are preserved, cestral form (i.e., atavism) in both the development and in the individ- they may provide an important macromorphological feature for deli- ual morphologies of the basal elements. On one hand, the apparently miting Dicroidium elongatum fronds from similar but unrelated fo- irregular development of modified basal elements itself can be inter- liage, such as czekanowskialean leaves (see, e.g., Harris, 1974)or preted as a functional and advantageous (see Section 4.5)atavisticex- the ginkgoalean species Sphenobaiera schenkii (Feistmantel) Florin pression. It is interesting to note that among seed ferns, similar basal and S. pontifolia Anderson et Anderson (see, e.g., Anderson and elements are so far only known to occur in fronds of the Palaeozoic Anderson, 1989). The characteristic morphology of the elements Medullosales (see Section 4.2). At the same time, however, it is also (e.g., Fig. 2) may also provide for identification of basal frond frag- worth mentioning that the remarkable morphological variety seen in ments in cases where other diagnostic criteria, such as the frond di- the basal frond outgrowths of Dicroidium includes several forms that chotomy or characteristic pinna morphologies, are not or only are reminiscent of individual pinnules of Palaeozoic seed–fern taxa, partially preserved. Anderson and Anderson (1983) introduced a sub- such as Rhacopteris Schimper (e.g., Walton, 1927), Nothorhacopteris species, D. elongatum subsp. dimorphum, based on the common occur- Archangelsky (e.g., Feistmantel, 1890; Archangelsky, 1983; White, rence of fronds with modified basal elements in the Molteno Formation of South Africa. The basal elements are, however, only in- consistently developed and show considerable variability among the different fronds (e.g., Plate I,1–11; see also Anderson and Anderson, 1983, pl. 54: Figs. 24–33, pl. 75: Figs. 1–9). Therefore, even though the informal morphological subgroups described here appear to occur in particular Dicroidium species, i.e., Type A elements in D. elongatum and D. crassinerve, and Type B elements in D. odontopteroides and D. dubium, respectively (see Fig. 1), the taxonomic significance of the modified basal elements for specific or infraspecific identification remains questionable. The overall foliar morphology of the basal elements is in many cases quite different from regular Dicroidium pinnules (Fig. 2). Thus, it seems likely that some early reports of isolated basal elements may not have been recognized as belonging to the Corystospermales. Fig. 3. Schematic drawings of laminar basal outgrowths on corystospermalean repro- The wedge-shaped outline, distally crenulate to divided margin, and ductive organs from the Upper Triassic Molteno Formation, South Africa. A, Ovulate evenly spreading venation of some specimens appears much more organ Pilophorosperma paucipartitum Thomas (=Umkomasia macleanii Thomas sensu similar to ginkgophyte foliage (see, e.g., Plate I,3–5, 8; Plate II, 2). In Anderson et Anderson 2003; redrawn from Thomas, 1933: Fig. 15). B, Ovulate organ Pilophorosperma gracile Thomas (=Umkomasia macleanii Thomas sensu Anderson et fact, the Australian D. elongatum fragment with basal elements Anderson 2003; redrawn from Thomas, 1933: Fig. 12). C, Pollen organ Pteruchus hoegii housed in the Paleobotanical Collections at KU was initially identified Thomas (=Pteruchus africanus Thomas sensu Anderson and Anderson, 2003; redrawn as a ‘dwarf leaf’ of Ginkgo digitata (Brongniart) Heer. from Thomas, 1933: Fig. 40). 24 B. 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1986), or Botrychiopsis Kurtz (e.g., Archangelsky and Arrondo, 1971). Is trees up to >30-m-tall (Cúneo et al., 2003; Taylor et al., 2006)that it therefore possible that, beyond the mere morphological similarity formed the dominant component of a warm-temperate polar forest (i.e., homoplasy), at least some of these early leaf-ontogenetic elements biome for which there are no modern analogs. Palaeogeographic recon- represent a re-emergence of ancestral foliage morphologies? At present structions place the Antarctic Dicroidium localities in the high-latitude we can only speculate about the potential significance of these struc- regions of southeastern Gondwana between 65° and 75°S (Scotese, tures, but we anticipate that future studies on the anatomy and leaf on- 2004; Veevers, 2004; Golonka, 2007; Torsvik et al., 2008). Regional cli- togeny of Dicroidium may ultimately provide sufficient information to mates during the Middle and Late Triassic are interpreted to have been determine whether in fact these basal foliar elements contain a phylo- warm-temperate and overall humid, with high rainfall throughout the genetically relevant signal. year (e.g., Parrish, 1990; Taylor et al., 2000; Preto et al., 2010). Season- A final aspect worth noting in this context is that modified foliar ality in these past polar forest biomes was, therefore, primarily con- outgrowths are also a conspicuous feature of reproductive organs in trolled by the annual photoperiodic fluctuation, with up to several the Corystospermales (Fig. 3; see, e.g., Thomas, 1933; Townrow, months of winter darkness and an equal period of continuous sunlight 1962; Holmes, 1987; Axsmith et al., 2000; Anderson and Anderson, during the growing season (see, e.g., Axelrod, 1984; Chaloner and 2003; Zan et al., 2008). In the ovulate organ Umkomasia Thomas Creber, 1989; Read and Francis, 1992; Taylor and Taylor, 1993; Creber emend. Klavins, these structures occur in the form of an opposite and Francis, 2003; Taylor and Ryberg, 2007).Asevidencedbyacombi- pair of basal bracts and isolated or paired bracteoles in proximal por- nation of tree-ring data, petiole anatomy, leaf phenology, and tapho- tions of more distal axes (see Thomas, 1933; Holmes, 1987; Axsmith nomic features, the Antarctic Dicroidium trees were seasonally et al., 2000; Klavins et al., 2002). Even though these outgrowths are in deciduous and survived the warm, dark polar winter by entering into most cases reduced to filiform appendages (see Thomas, 1933; a state of dormancy (Taylor, 1989, 1996; Meyer-Berthaud et al., 1992; Holmes, 1987; Anderson and Anderson, 2003), they may also attain Taylor and Taylor, 1993; Cúneo et al., 2003; Taylor and Ryberg, 2007; a much more leaf-like and partially sheathing morphology that is Bomfleur and Kerp, 2010). reminiscent of some of the basal frond elements described here We offer the hypothesis that the modified basal elements in (Fig. 1A, B; see, e.g., Thomas, 1933: Figs. 8, 12, 14a, 15). Moreover, Dicroidium were the initial, more or less irregularly enlarged foliar similar to the present material, the inconsistent occurrence of the outgrowths of spring flush. Apart from providing a protective cover modified outgrowths on Umkomasia has been interpreted as a result for the developing frond blade, enlarged laminar outgrowths at the of the ephemeral nature of these structures (Holmes, 1987). We sug- beginning of the growing season would have provided an increased gest that the same may also apply to the pollen organ Pteruchus, a few energy boost early in the spring. The teeth in some temperate-zone, of which have been reported to bear small, modified foliar out- toothed leaves perform a similar function today by providing a site growths at or near the base (Fig. 3C; see Thomas, 1933; Townrow, of early-season photosynthesis before the remainder of the leaf ex- 1962). Townrow (1962, p. 315) interpreted these structures as re- pands (Baker-Brosh and Peet, 1997; Royer et al., 2009). Moreover, duced pinnae based on the similarity to the modified basal elements the immediate availability of a large leaf-surface area would have in different Dicroidium fronds, and concluded that Pteruchus likely also increased the transpirational pull necessary for a rapid re- represented a modified leaf. A later study on structurally preserved initiation of sap flow. This latter functional aspect may have been of Pteruchus organs from Antarctica, however, demonstrated a stem- special importance, given that the Dicroidium trees produced consid- like anatomy of the main axis with helically arranged microsporo- erable stem wood volume (Cúneo et al., 2003; Taylor and Ryberg, phylls (Yao et al., 1995), supporting Thomas' (1933) initial interpre- 2007) that remained quiescent for several months during winter tation of Pteruchus as a fertile branching system. Regardless of how dormancy. the structural relationships or possible homologies of the modified foliar elements among these different organs may be interpreted, it appears that the ability to produce caducous, modified foliar outgrowths Acknowledgments is a distinctive character not only of the foliage, but also of other organs in the Gondwanan Dicroidium plants. We thank Anne-Laure Decombeix (Lawrence, KS), Rudolph Serbet (Lawrence, KS), and Rubén Cúneo (Trelew, Chubut, Argentina) for 4.5. Possible ecological function valuable discussions, and gratefully acknowledge technical assistance by Carla J. Harper (Lawrence, KS). Helpful comments and suggestions It is generally assumed that the main functions common to cyclop- by Michael Krings (München) and an anonymous reviewer are grate- teri(o)d elements on seed–fern fronds, aphlebiae of fossil ferns, and fully acknowledged. Financial support has been provided by the Alex- enlarged laminar stipules in angiosperms are to provide physical pro- ander-von-Humboldt Stiftung (Feodor Lynen Fellowship to B.B.) and tection and an appropriate moist microenvironment for the young the National Science Foundation (NSF grant ANT-0943934 to E.L.T. developing leaf (see, e.g., von Roehl, 1868; Stur, 1875; Lubbock, and T.N.T.). 1899; Goebel, 1898–1901; Potonié, 1903; Bower, 1910; Sinnott and Bailey, 1914; Florin, 1925; Hirmer, 1927; Majumdar, 1956; Crookall, 1959; Laveine, 2005; Phillips and Galtier, 2005, 2011). In addition, en- References larged stipules in certain angiosperm leaves may contribute signifi- Abu Hamad, A., Kerp, H., Vörding, B., Bandel, K., 2008. A Late Permian flora with Dicroidium cantly to photosynthesis; an extreme example is the extant legume from the Dead Sea region, Jordan. 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