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respect to leaf architecture and epidermal characters by LM and SEM. The leaf venation of Zelkova is relatively uniform, while leaf size and shape are highly ...

Botanical Journal of the Linnean Society (2001), 136: 255–265. With 41 figures doi:10.1006/bojl.2000.0432, available online at http://www.idealibrary.com on

Leaf architecture and epidermal characters in Zelkova, Ulmaceae YU-FEI WANG∗1, DAVID K. FERGUSON2, REINHARD ZETTER2, THOMAS DENK3 and GIUSEPPE GARFI4 1

Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China Institut fu¨r Pala¨ontologie, Universita¨t Wien, Geozentrum, Althanstrasse 14, A-1090 Wien, Austria 3 Swedish Museum of Natural History, Department of Paleobotany, Box 50007, S-104 05 Stockholm, Sweden 4 Via IV novembre 38, I-96010 Buccherri (SR), Italy 2

Received April 2000; accepted for publication August 2000

Zelkova, with six extant species in Eurasia – three in East Asia (Z. schneideriana, Z. serrata, Z. sinica), one in south-western Asia (Z. carpinifolia) and two in southern Europe (Z. abelicea, Z. sicula) – was investigated with respect to leaf architecture and epidermal characters by LM and SEM. The leaf venation of Zelkova is relatively uniform, while leaf size and shape are highly variable. Characters such as teeth and epidermal cells, trichomes and stomata provide useful specific distinctions. Beginning in the Miocene, increasing aridity in Central Asia would appear to have been responsible for isolating the eastern Asiatic species from their European/western Asiatic counterparts. The European range underwent further changes in response to Quaternary climatic oscillations.  2001 The Linnean Society of London

ADDITIONAL KEY WORDS: stomata – teeth – trichomes – wax.

The genus Zelkova consists of six extant species of temperate trees in Eurasia, three (Z. schneideriana, Z. serrata, Z. sinica) in East Asia (Chen, 1998), one (Z. carpinifolia) in south-western Asia (Gagnidze, 1975; Czerepanov, 1995) and two (Z. abelicea and Z. sicula) in southern Europe (Sarlis,1987; Di Pasquale et al., 1992). Zelkova is an accessory element of north temperate forests, and was once widespread in the Tertiary of the Northern Hemisphere. The fossil record consists of numerous leaves, pollen grains and some drupaceous fruits (Buzek, 1971; Manchester, 1989). In the past, identification of fossil species in Zelkova was mainly based on the gross morphology of leaves. This led to the establishment of many fossil species of doubtful validity, because a true understanding of the variation in leaf architecture and epidermis in the genus was lacking (Buzek, 1971; Burnham, 1986a, b). Recently, cuticles have been obtained from fossil Zelkova leaves (Hably, 1997). Therefore, a revision of Czerepanov’s review of the genus (1957), utilizing micromorphological features, had become essential in order to compare them to fossil taxa. Without this biological information, tracing the evolutionary history

INTRODUCTION The Ulmaceae, or elm family, is traditionally divided into two subfamilies, Ulmoideae and Celtidoideae, covering 18 genera (15 extant, three extinct) and about 150 species (Cronquist, 1981; Manchester, 1989; Todzia, 1993) although some authors suggest that Celtidoideae can be separated from Ulmaceae and elevated to Celtidaceae (Wiegrefe, Sytsma & Guries, 1998). The Ulmoideae differs from the Celtidoideae in having a generally craspedodromous rather than brochidodromous venation pattern, and a samara as opposed to a drupaceous fruit type. However, the genus Zelkova, which is placed in the Ulmoideae, has a craspedodromous venation pattern found in the Ulmoideae and a fruit similar to that of the Celtidoideae. Thus it differs from all the other genera in the Ulmaceae. This unique combination of fruit and leaf characters provides a precise clue for the identification of fossil Zelkova (Manchester, 1989).

∗ Corresponding author. E-mail: [email protected] 0024–4074/01/070255+11 $35.00/0

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 2001 The Linnean Society of London

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of Zelkova, and establishing the relationships of fossil taxa to living counterparts, are likely to prove difficult. The aim of this paper is to provide the necessary data and thus contribute to a better understanding of evolution in Zelkova.

MATERIAL AND METHODS The herbarium sheets examined originated from PE, Institute of Botany, Chinese Academy of Sciences (CAS), Institut fu¨r Botanik, Universita¨t Wien (WU), and field collections by Thomas Denk and Giuseppe Garfi. The list of voucher specimens is as follows: Z. schneideriana Hand.-Mazz.: Bartholomew et al., 1855 (PE), C. W. Wang, 87734 (PE), F. Z. Wang, 10907 (PE), Anon, 022 (PE); Z. serrata (Thunb.) Makino: C. Y. Chiao, 2453 (PE), K. Chen, 145 (PE), K. T. Fu, 2554 (PE), Anon, 68 (PE), Anon, 29680 (PE); Z. sinica C. K. Schneider: K. J. Guan, 6030 (PE), K. R. Liu, 29 (PE); Z. carpinifolia (Pall.) K. Koch: T. Denk, 89650, 99618, 99619; Z. abelicea (Lam.) Boiss: A. Baldacci, 143 (WU); Z. sicula Di Pasquale, Garfi et Quezel: G. Garfi s.n. Leaves were cleared using a 10% solution of NaOH. Cuticles were prepared using Schulze’s solution (HNO3 and KClO3 mixed at 5:1). Standard procedures were followed for SEM. The specimen samples were fixed to a labelled stub, coated with gold using a sputter coater, and scanned with a JSM-6400 Scanning Electron Microscope. The terminology used is that of Hickey (1979) for leaf architecture and Dilcher (1974) for cuticle analysis.

Epidermal characters Epidermal cells with undulate, rounded or straight anticlinal walls (Figs 36–41) except over veinlets where they are elongate and straight. On the upper epidermal surface, the indumentum consists of spinose, unicellular hairs of variable length, all with expanded base, and sometimes scattered glandular multicellular hairs (Figs 18, 20, 22, 24, 26, 28). Trichomes of two types on the lower epidermis: non-glandular unicellular hairs (Figs 18, 20, 22, 24, 26, 28, 35) and glandular multicellular hairs, each with an apical gland, a neck cell, a stalk cell and a basal cell (Figs 23, 30, 34). Hair bases surrounded by a zone of radiating epidermal cells (Figs 36, 37, 39, 41). Stomata anomocytic, confined to the lower surface of epidermis (Figs 19, 21, 23, 25, 27, 29–33). SPECIFIC DIFFERENCES

Z. schneideriana Hand.-Mazz Primary vein bearing 8–16 pairs of secondary veins. Teeth fine and shallow, on basal side convex to acuminate, apical side straight to acuminate, tooth shape serrate, tooth apex acute (Figs 1, 2, 10, 18). Epidermal cells with undulate anticlinal walls (Fig. 36); stomatal distribution equidistant (Fig. 19). The distribution of unicellular, non-glandular, spinose and multicellular, glandular hairs roughly equidistant (Figs 18, 35). Z. serrata (Thunb.) Makino

RESULTS GENERIC DESCRIPTION

Leaf architecture Leaves alternate, simple with petiole. Lamina ovate, elliptical or lanceolate, leaf base asymmetrical or symmetrical, cuneate, rounded, or cordate. Leaf apex acute to acuminate or obtuse to rounded (Figs 1–9). Leaf margin serrate, simple toothed, tooth axis central to excentric (Figs 1–12, 14, 15, 17), 3° and 4° accessory veins around the tooth axis looped (Figs 10–17). Individual teeth occasionally bearing a subsidiary tooth (Figs 1, 2, 5, 6). Venation pinnately craspedodromous: primary vein straight or curved distally, secondary vein curving upwards and entering the teeth excentrically or subcentrally, sometimes dichotomizing or fusing at some distance from the midvein (Figs 1–9). Tertiary veins arising from secondary vein at about 90°, non-percurrent, quaternary veins arising from the tertiary veins at about 90°, usually 3°, 4° or 5° veins forming angular network (Figs 1–17). Areoles welldeveloped, polygonal, free vein-endings multibranched (Figs 10–17).

Primary vein bearing 7–15 pairs of secondary veins. Teeth fine and shallow, on both basal and apical sides acuminate, tooth shape serrate, tooth apex acuminate (Figs 4, 5, 11, 20). Epidermal cells with straight or rounded anticlinal walls (Fig. 37). Stomatal distribution equidistant (Fig. 21). Striae present around stomata (Fig. 21). The distribution of unicellular, non-glandular, spinose and multicellular, glandular hairs roughly equidistant (Fig. 20). Z. sinica C. K. Schneid. Primary vein bearing 4–12 pairs of secondary veins. Teeth fine and shallow, on both basal and apical sides convex, tooth shape crenate, tooth apex obtuse (Figs 3, 12, 22). Epidermal cells with straight anticlinal walls (Fig. 38). Stomatal distribution clustered (Figs 23, 30). Striae present around stomata (Fig. 23). Distribution of unicellular, non-glandular, spinose hairs roughly equidistant while multicellular, glandular hairs highly clustered around stomata on the lower surface of epidermis (Figs 22, 23, 30–31).

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Figures 1–9. Cleared leaves of Zelkova. Scale bar=1 cm. Figs 1, 2. Z. schneideriana. Botanical Garden, CAS, Beijing. Fig. 3. Z. sinica. Coll. K. J. Guan 6030 (PE). Fig. 4. Z. serrata. Coll. C. Y. Chiao 2453 (PE). Fig. 5. Z. serrata. Botanical Garden, CAS, Beijing. Fig. 6. Z. sicula. Coll. G. Garfi s.n. Fig. 7. Z. carpinifolia. Coll. T. Denk 89650. Fig. 8. Z. carpinifolia. Coll. T. Denk 99618. Fig. 9. Z. abelicea. Coll. A. Baldacci 143 (WU).

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Figures 10–17. Details of leaf architecture and tooth structure of Zelkova. Scale bar=1 mm. Fig. 10. Z. schneideriana. Botanical Garden, CAS, Beijing. Fig. 11. Z. serrata. Coll. C. Y. Chiao 2453 (PE). Fig. 12. Z. sinica. Coll. K. J. Guan 6030 (PE). Fig. 13. Z. serrata. Coll. C. Y. Chiao 2453 (PE). Fig. 14. Z. carpinifolia. Coll. T. Denk 89650. Fig. 15. Z. abelicea. Coll. A. Baldacci 143 (WU). Fig. 16. Z. carpinifolia. Coll. T. Denk 89650. Fig. 17. Z. sicula Coll. G. Garfi s.n.

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Figures 18–23. Epidermal characters of eastern Asiatic species of Zelkova. Fig. 18. Z. schneideriana. Upper epidermis of tooth displaying spinose, unicellular hairs. Coll. F. Z. Wang 10907 (PE). Scale bar=0.1 mm. Fig. 19. Z. schneideriana. Detail of three stomata on lower epidermis. Coll. F. Z. Wang 10907 (PE). Scale bar=10 m. Fig. 20. Z. serrata. Upper epidermis of tooth displaying spinose, unicellular hairs. Coll. C. Y. Chiao 2453 (PE). Scale bar=0.1 mm. Fig. 21. Z. serrata. Lower epidermis with striae round stomata. Coll. C. Y. Chiao 2453 (PE). Scale bar=10 m. Fig. 22. Z. sinica. Upper epidermis of tooth displaying spinose, unicellular hairs. Coll. K. J. Guan 6030 (PE). Scale bar=0.1 mm. Fig. 23. Z. sinica. Lower epidermis with stomata, glandular hairs and striae. Coll. K. J. Guan 6030 (PE). Scale bar=10 m.

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Figures 24–29. Epidermal characters of European and western Asiatic species of Zelkova. Fig. 24. Z. carpinifolia. Upper epidermis of tooth displaying spinose, unicellular hairs. Coll. T. Denk 89650. Scale bar=0.1 mm. Fig. 25. Z. carpinifolia. Detail of two stomata displaying thickened poral wall and striae. Coll. T. Denk 89650. Scale bar=10 m. Fig. 26. Z. abelicea. Upper epidermis of tooth displaying spinose, unicellular hairs. Coll. A. Baldacci 143 (WU). Scale bar=0.1 mm. Fig. 27. Z. abelicea. Lower epidermis with stomata and wax layer. Coll. A. Baldacci 143 (WU). Scale bar=10 m. Fig. 28. Z. sicula. Upper epidermis of tooth, displaying spinose, unicellular hairs with swollen bases. Coll. G. Garfi s.n. Scale bar=0.1 mm. Fig. 29. Z. sicula. Lower epidermis with three stomata and scattered, granular wax. Coll. G. Garfi s.n. Scale bar=10 m.

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Figures 30–-35. Details of the epidermis under SEM of Zelkova. Fig. 30. Z. sinica. Lower epidermis displaying clustered stomata and glandular trichomes. Coll. K. J. Guan 6030 (PE). Scale bar=100 m. Fig. 31. Z. sinica. Detail of two stomata, striae and glandular hairs. Coll. K. J. Guan 6030 (PE). Scale bar=10 m. Fig. 32. Z. abelicea. Lower epidermis with stoma surrounded by needle-shaped wax. Coll. A. Baldacci 143 (WU). Scale bar=10 m. Fig. 33. Z. sicula. Lower epidermis with stoma and granular wax. Coll. G. Garfi s.n. Scale bar=10 m. Fig. 34. Z. sicula. Detail of glandular hair. Coll. G. Garfi s.n. Scale bar=10 m. Fig. 35. Z. schneideriana. Upper epidermis displaying unicellular trichomes of various lengths. Coll. F. Z. Wang 10907 (PE). Scale bar=100 m.

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Figures 36–41. Detailed characters of anticlinal walls of epidermal cells on upper epidermis of Zelkova. Scale bar= 20 m. Fig. 36. Z. schneideriana. Botanical Garden, CAS, Beijing. Fig. 37. Z. serrata. Coll. C. Y. Chiao 2453 (PE). Fig. 38. Z. sinica. Coll. K. J. Guan 6030 (PE). Fig. 39. Z. carpinifolia. Coll. T. Denk 89650. Fig. 40. Z. abelicea. Coll. A. Baldacci 143 (WU). Fig. 41. Z. sicula Coll. G. Garfi s.n.

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Table 1. Key to species of Zelkova based on leaf characters 1. Teeth fine with shallow sinuses .................................................................................................................................................. 2 2. Teeth crenate, their apices obtuse, stomata and multicellular hairs clustered ..................................................... Z. sinica 2. Teeth serrate, their apices acute or acuminate, stomata and multicellular hairs±equidistant ....................................... 3 3. Tooth apex acute, anticlinal cell walls undulate, stomata not surrounded by striae ........................... Z. schneideriana 3. Tooth apex acuminate, anticlinal cell walls straight or rounded, stomata surrounded by striae ................... Z. serrata 1. Teeth coarse with deep sinuses ................................................................................................................................................... 4 4. Leaves with (3–) 6–12 pairs of veins, leaf base toothed, tooth apex acute, anticlinal cell walls undulate . Z. carpinifolia 4. Leaves with 3–8 pairs of veins, leaf base entire, tooth apex obtuse to rounded, anticlinal cell walls rounded ............... 5 5. Bases of unicellular hairs on upper leaf surface swollen, wax on lower surface scattered, granular, tooth apex±mucronate ..................................................................................................................................................... Z. sicula 5. Bases of unicellular hairs on upper leaf surface not swollen, wax on lower surface dense, needle-like, tooth apex nonmucronate .............................................................................................................................................................. Z. abelicea

Table 2. Leaf architecture and epidermal characters in Zelkova

No. of secondaries (pairs)

Z. schneideriana

Z. serrata

Z. sinica

8–16

7–15

4–12

fine, shallow convex to acuminate straight to acuminate serrate acute

fine, shallow acuminate acuminate serrate acuminate

fine, shallow convex convex crenate obtuse

undulate equidistant absent absent equidistant equidistant

straight to rounded equidistant present absent equidistant equidistant

straight clustered present absent clustered clustered

Z. carpinifolia

Z. abelicea

Z. sicula

3–12

3–6

3–8

coarse, deep convex onvex serrate acute

coarse, deep slightly convex slightly convex crenate obtuse to rounded

coarse, deep slightly convex slightly convex crenate obtuse

undulate equidistant present absent equidistant equidistant

rounded equidistant absent present equidistant equidistant

rounded equidistant absent present equidistant equidistant

TOOTH ARCHITECTURE

tooth type basal side apical side shape apex EPIDERMAL CHARACTERS

anticlinal walls stomatal distribution striae wax ornamentation distrib. of unicellular hairs distrib. of multicellular hairs

No. of secondaries (pairs) TOOTH ARCHITECTURE

tooth type basal side apical side shape apex EPIDERMAL CHARACTERS

anticlinal walls stomatal distribution striae wax ornamentation distrib. of unicellular hairs distrib. of multicellular hairs

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Z. carpinifolia (Pall.) K. Koch Primary vein bearing 3–12 pairs of secondary veins. Teeth coarse and deep, on both basal and apical sides convex, tooth shape serrate, tooth apex acute (Figs 7, 8, 14, 24). Epidermal cells with remarkably undulate anticlinal walls (Fig. 39). Stomatal distribution equidistant. Striae present around stomata (Fig. 25). The distribution of unicellular, non-glandular, spinose and multicellular, glandular hairs roughly equidistant (Figs 24, 25). Z. abelicea (Lam.) Boiss. Primary vein bearing 3–6 pairs of secondary veins. Teeth coarse and deep, on both basal and apical sides slightly convex, tooth shape crenate, tooth apex obtuse to rounded (Figs 9, 15). Epidermal cells with rounded anticlinal walls (Fig. 40); stomatal distribution equidistant (Fig. 27). A dense, needle-like wax ornamentation present on the lower epidermis (Figs 27, 32). The distribution of unicellular, non-glandular, spinose and multicellular, glandular hairs roughly equidistant (Fig. 26). Z. sicula Pasquale, Garfi & Quezel Primary vein bearing 3–8 pairs of secondary veins. Teeth coarse and deep, on both basal and apical sides slightly convex, tooth shape crenate, tooth apex obtuse (Figs 6, 17, 28). Epidermal cells with rounded anticlinal walls (Fig. 41); stomatal distribution equidistant (Fig. 29). The distribution of unicellular, non-glandular, spinose and multicellular, glandular hairs roughly equidistant (Fig. 28). For key to species, see Table 1.

DISCUSSION The species of Zelkova possess a number of unifying characters, such as their simple leaves with craspedodromous venation and simple toothed margin. The epidermis displays two types of trichomes: nonglandular, unicellular hairs and glandular multicellular hairs and anomocytic stomata limited to the lower leaf surface. These common features can be considered to reflect the close affinities among the species and imply a monophyletic origin. With the exception of the tooth structure, the characters of leaf architecture provide few features of taxonomic value in the separation of the different species, which explains why Czerepanov (1957) was unable to distinguish clearly between the species. Epidermal features provide enough information to clearly distinguish between the six extant species of

Zelkova (Table 2). Stomatal distribution and arrangement of multicellular hairs on the lower leaf surface appear to be correlated, and distinguish Zelkova sinica from all the remaining species (clustered vs. equidistant distribution). By contrast, the significance of the degree of undulation of the anticlinal cell walls remains to be proven by studying intraspecific variation (e.g. sun leaves vs shade leaves). For example, the leaves of Zelkova carpinifolia investigated originated from the shade leaves of a plant growing under a humid climate with c. 2700 mm precipitation per year. This could induce the conspicuous undulation of the anticlinal cell walls. Both Mediterranean species (Z. abelicea, Z. sicula) display rounded epidermal cells, which might be a response to strong insolation. High levels of evapotranspiration in the growing season explain why the leaves of these species are small, with only a few pairs of secondary veins. The needle-like wax ornamentation, which distinguishes Zelkova abelicea from all the other species, may represent an adaptation to a summer-dry Mediterranean climate, just as submediterranean, thermophilous Quercus pubescens differs from temperate Q. petraea by its persistent trichomes and wax ornamentation on the lower epidermis. All the eastern Asiatic species possess shallow sinuses, while western Asiatic and European species have coarse teeth. This might indicate that the eastern Asiatic and European populations have been isolated for a long period of time. A disjunction between these populations would appear to have arisen in the Middle Miocene as a result of increasing aridity in Central Asia (Ferguson, Liu & Zetter, 1997). However, the genus continued to be widespread in Europe/western Asia, and East Asia until the beginning of the Pleistocene. The Pleistocene ice ages caused widespread cooling and aridity. In Europe Zelkova, along with other mesophytic trees, became restricted to refugia. During the interglacial periods Zelkova would have been able to expand. However, because the short shoots with drupaceous fruits only travel a few metres from the trees (Hoshino, 1993), this expansion was slow. As a result, Zelkova was continuously forced to compete for space with earlier immigrants. This and a number of natural barriers (rivers, channels etc.) limited the extent of its area. It was still present in southern France at the end of the Early Pleistocene (c. 900 Ka; Ablin, 1991) and probably persisted into the Middle Pleistocene. At that time it was still present on mainland Greece. It finally disappeared some time after 440 Ka (Van der Wiel & Wijmstra, 1987). However, it persisted in central Italy until shortly before 31 Ka (Follieri, Magri & Sadori, 1986). As its area continued to shrink, and the number of individuals diminished, the chances of genetic drift increased. As pointed out above, the

LEAF ARCHITECTURE AND EPIDERMIS IN ZELKOVA

establishment of a summer dry climate in the Mediterranean area in the Quaternary would have had a direct impact on the leaf physiognomy of the remaining populations on Crete and southeast Sicily (Sarlis, 1987; Di Pasquale et al., 1992; Nakagawa et al., 1998).

ACKNOWLEDGEMENTS We thank Prof. Fu D.-Z, Dr Qin H.-N, at PE, Institute of Botany, Chinese Academy of Sciences and Dr Walter Till, Institute of Botany, University of Vienna for permitting the study of their herbarium sheets. Profs Chen C.-J, Ying J.-S, Li Z.-Y and Fu L.-G (PE) provided many helpful suggestions on the revision of our manuscript. Thanks are due to Ms Heidelinde Karam, Ms Ursula Juszczak and Mr Rudolf Gold at the Institute of Palaeontology, University of Vienna, for their kind assistance. The work was supported by National Natural Science Foundation of China (Nos 39930020, 39300007, 30070046 & 39770054), Chinese Academy of Sciences (Project KZ951-B1-105, STZ-1-01, STZ-0030 & SFPPAS) and the scholarship program 894/96 ¨ AD to Yu-Fei Wang during his stay in Vienna. from O

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