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Eostangeria Ruzinciniana (Zamiaceae) from the Middle Miocene of Bulgaria and Its Relationship to Similar Taxa of Fossil Eostang

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Eostangeria Ruzinciniana (Zamiaceae) from the Middle Miocene of Bulgaria and Its Relationship to Similar Taxa of Fossil Eostang Acta Palaeobot. 41(2): 177–193, 2001 Eostangeria ruzinciniana (Zamiaceae) from the Middle Miocene of Bulgaria and its relationship to similar taxa of fossil Eostangeria, and extant Chigua and Stangeria (Cycadales) KRASSIMIRA UZUNOVA1, EMANUEL PALAMAREV2 and ZLATKO KVACˇ EK3 1 Biological Faculty, Sofia University, 8 Dragan Znakov, 1421 Sofia, Bulgaria 2 Institute of Botany, Bulgarian Academy of Sciences, 23 Acad. G. Bonchev, 1113 Sofia, Bulgaria, e-mail: [email protected] 3 Charles University, Faculty of Science, Albertov 6, 128 43 Praha 2, Czech Republic, e-mail: [email protected] Received 13 November 2000; accepted for publication 3 Mai 2001 ABSTRACT. Characterisation of Eostangeria ruzinciniana (Palamarev, Petkova & Uzunova) Palamarev & Uzu- nova (Middle Miocene – Volhynian, Bulgaria) is augmented. The species is compared with morphologically simi- lar cycads: E. saxonica Barthel (Eocene of Germany), E. pseudopteris Z. Kvacˇek & Manchester (Late Palaeocene and Eocene of western USA), and the extant Chigua D. Stevenson and Stangeria T. Moore. Leaf epidermal anatomy indicates that E. ruzinciniana is closely related to other members of Eostangeria, forming with them a natural unit. Eostangeria slightly differs from Chigua (Zamioideae) in the presence of short dark-staining cells in the lower epidermis, densely toothed margins, and in the case of Eostangeria ruzinciniana by obviously per- sistent, non-articulated leaflets. In morphological features of the leaflets, Eostangeria resembles Stangeria (Stangeriaceae); however, the latter decidedly differs in entirely cyclocytic stomata lacking ventral lignified la- mellae, coarsely striated epidermis with strongly undulate anticlines and an absence of short dark-staining cells. A new subfamily Eostangerioideae is suggested to accommodate Eostangeria within Zamiaceae. KEY WORDS: leaf anatomy, Cycads, Zamiaceae, Eostangerioideae, palaeoecology, Tertiary INTRODUCTION Discovery of every new taxon of fossil or re- and discovery of a new recent genus Chigua cent cycads is of interest for deciphering evol- (Stevenson 1990) give a new stimulus for fur- ution of this plant group. The cycads combine ther comparative investigation of these cycads. important morphological and anatomical fea- In this paper, we summarize the results tures that help elucidate evolution and adap- from a reinvestigation of all samples of Eos- tations of the gymnosperms in general. In re- tangeria ruzinciniana (Palamarev, Petkova cent floras, the cycads are characterized by & Uzunova) Palamarev and Uzunova in detail highly disjunct distribution ranges and pro- and compare the species with the other extinct nounced endemism. The roots of these pecu- species of Eostangeria Barthel and repre- liarities have to be traced in the past history of sentatives of the recent genera Stangeria T. this group. Moore and Chigua D. Stevenson. The recognition of a new extinct species of the fossil genus Eostangeria in western North MATERIAL AND METHODS America (Kvacˇek & Manchester 1999) after The fossil samples of Eostangeria ruzinciniana (Pa- E. saxonica (Barthel 1976) and E. ruzincinia- lamarev, Petkova & Uzunova) Palamarev and Uzunova na (Palamarev & Usunova 1992) in Europe came from the Lower Sarmatian, i.e., Volhynian sedi- 178 ments (Middle Miocene) of the Krivodol Formation in ruzinciniana, Stangeria eriopus, Chigua re- northwestern Bulgaria near the village of Ružinci (co- strepoi ) to the linear-lanceolate shape (Chigua ordinates lat. 43°40′ N, long. 23°20′ E). This site is the only place, where E. ruzinciniana has been recovered. bernalii) with the intermediate form (oblong- Fragments of pinnate leaves studied (samples No. lanceolate) ocurring in Eostangeria pseudop- 3517, 3518, 3615, 3657) are preserved in marly sandy teris and Stangeria eriopus. The leaflets show shale as impressions with preserved cuticles. The great size variation. The fossil species E. sax- slides with cuticular membranes (Nos 21, 28, 34, 39, onica and E. pseudopteris have similar dimen- 44a, 46, 60, 61 and 61a) were prepared from the sample No. 3518. The comparative material of recent sions of the leaflets while E. ruzinciniana dif- cycads has been studied in the herbaria and on plants fers from them in its shorter and slender lea- in cultivation (National Museum of Natural History, flets (about 60 mm long and 5–10 mm wide). Washington, DC (USNM), New York Botanical Garden The two species of the recent genus Chigua (NY), botanical gardens Berlin-Dahlem and Gaines- and Stangeria eriopus possess much larger ville). Anatomical slides belong to the collections of the Department of Palaeobotany and Pollen Analysis of leaflets than all the fossil taxa of Eostangeria the Botanical Institute of Bulgarian Academy of Scien- (Tab. 1 and Fig. 1a, b). ces (Nos 2627, 2628 2629, 2630, 2631, 2632, 2633) and Faculty of Science, Charles University, Prague. Leaf ATTACHMENT fragments for anatomical observation have been ob- tained from Chigua restrepoi (D. Stevenson 693, NY) Leaflets of Eostangeria ruzinciniana are al- and C. bernalii (Bernal, Galeano Restrepo 1189, ways fossilized together with the rachis (Pl. 1 USNM), the specimens of Stangeria eriopus came from figs 1–2, 4). This is an indication they may not the cultivated plants in the Botanical Garden Berlin- Dahlem (E. Palamarev 2604), and Gainesville, those of be deciduous and the pinnate leaf has prob- Zamia and Ceratozamia from the collection of Florida ably fallen completely. The other species of University (G. Schutzman, Gainesville). Eostangeria have been found always as de- The descriptions of morphological and anatomical tached leaflets, a possible evidence that they characters follow the terminology of Pant and Nau- were articulate (as is the case in all Zamioi- tiyal (1963) and Dilcher (1974). Preparations of cuticular membranes were made by deae incl. Chigua). The leaflets of Stangeria maceration in Schulze solution followed by clearing in are not deciduous from the rachis. 5% KOH or by treatment in 20% hydrogen peroxide. Most of the cuticular membranes have been stained in VENATION Sudan IV, or safranine. All species compared have more or less fre- quently dichotomizing secondary veins and the COMPARATIVE MORPHOLOGICAL venation is basically pinnate craspedodromous DATA OF LEAFLETS and camptodromous. In some species, the veins terminate in the leaflet teeth but in Eos- FORM AND SIZE tangeria ruzinciniana, Chigua restrepoi and C. bernalii the veins are faintly visible before en- Eostangeria, Chigua and Stangeria all pos- tering the teeth or join the margin (Pl. 1 fig. 3). sess fernlike leaves with a stout rachis and In Eostangeria pseudopteris (like in Stange- leaflets with pinnate venation (Fig. 1a-f). The ria), a peculiar looping (fusing) of two adjacent leaflets are opposite to predominantly alter- secondaries on the leaf margin was rarely ob- nate. Eostangeria ruzinciniana has markedly served (Kvacˇek & Manchester 1999). spiral arrangement but in the other two fossil In Stangeria, Eostangeria, and Chigua re- species of the genus Eostangeria the phyllo- strepoi the midrib reaches the leaflet apex, taxy is unknown. In the recent species Stange- while in C. bernalii, it splits into individual ria eriopus both types of the leaflet arrange- veins within its course and loses its individ- ment can be observed (Greguss 1968). The uality before reaching the leaflet tip (Fig. 1a). species of Chigua also have mixed arrange- These species can be further differentiated ments, being spiral on the base of the rachis, into two groups according to the density and almost opposite in the middle part of the ra- angle of divergence of the secondaries: a group chis and opposite in the upper part (Stevenson with more than 15 pairs of secondaries and 1990). These data show that the arrangement wide angles (50–75°) – Eostangeria saxonica, of leaflets lacks any taxonomic value. E. pseudopteris and Stangeria eriopus, and According to the form of leaflets, we can rec- a group with only 10–15 pairs of veins and ognize a range from lanceolate (E. saxonica, E. narrow angles (less than 50°) – Eostangeria Table 1. Morphological features of the leaflets of Eostangeria, Chigua and Stangeria Number and Termination of Species Form Base Apex Margin Midvein angle of Size (in cm) secondaries secondaries Eostangeria saxonica lanceolate asymmetric acute toothed prominent more than 25 ±every third vein 12.0×1.6 Barthel cuneate sessile irregularly along pairs, dichotomic terminates in the whole leaflet 60–75°, alternate a tooth length E. ruzincianiana lanceolate asymmetric acute regularly toothed, moderate about 15 pairs ±every second 5.0–7.0×1.0–2.0 (Palamarev, Petkova & cuneate- the base entire dichotomic vein terminates Uzunova) Palamarev & decurrent, sessile 40–50°, alternate obscurely in Uzunova a tooth E. pseudopteris oblong- lanceolate asymmetric attenuate irregularly moderate more than 25 ±every second 11.0×2.0–3.0 Z. Kvacˇek & Manchester cuneate sessile or toothed, the base paires, mostly vein terminates short petiolulate entire simple 60–75°, obscurely in opposite or a tooth alternate Chigua restrepoi lanceolate to symmetric acute irregularly moderate weak about 10–12 most secondaries 15.0–25.0×3.0–5.0 D. Stevenson lanceolate-ovate cuneate sessile toothed, the base pairs, mostly terminate entire simple 2–30°, obscurely in alternate widely spaced teeth C. bernalii D. Stevenson linear- lanceolate symmetric attenuate irregularly moderate, not about 10–15 most secondaries 30.0–35.0×1.0–1.5 cuneate sessile toothed, the base
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