Sclerotesta morphology and its systematic implications in magnoliaceous seeds

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1 Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society The Linnean Society of London, 2003? ? Original Article SCLEROTESTA MORPHOLOGY F.-X. XU Botanical Journal of the Linnean Society, 2003, 142, With 71 figures Sclerotesta morphology and its systematic implications in magnoliaceous seeds FENG-XIA XU* South China Institute of Botany, Academia Sinica, Guangzhou , China Received October 2002; accepted for publication February 2003 Seeds of 101 species from 14 genera were observed using stereoscopic and scanning electron microscopy. Sclerotesta morphology is stable within the genera of Magnoliaceae. Two different morphological types are described according to features of the chalazal region, which have great value in classification and have been found only in Magnoliaceae. One is the pore type, characterized by being simple, observed in the relatively primitive taxa of this family, including Manglietia, Pachylarnax, Magnolia (19 species), Aromadendron, Talauma (eight species), Parakmeria (one species), Kmeria (one species), Elmerrillia and Liriodendron. The other one is the tube type, which is characterized by having a more complex structure consisting of a central hollow tube contained within a hole. This type was observed in relatively advanced taxa, including Manglietiastrum, Magnolia (15 species), Talauma (three species), Parakmeria (four species), Kmeria (one species), Alcimandra, Michelia, Paramichelia and Tsoongiodendron. Transitional types between these two were observed in some species of Magnolia. Chalazal region morphology, together with other useful sclerotesta characters, including seed size, shape, the raphal sinus and the external surface of the sclerotesta, may be used as diagnostic characteristics of genera, and even species in Magnoliaceae. A key to identify the different genera is supplied The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, ADDITIONAL KEYWORDS: diagnostic characteristics Magnoliaceae morphology sclerotesta. * xfx@scib.ac.cn INTRODUCTION The seed coats of Magnoliaceae comprise both exterior sarcotesta and interior sclerotesta. The former contains exotesta and mesotesta and the latter is part of the sclerotesta. Seed morphology is a useful character and has been utilized in the identification of fossil and modern magnoliaceous seeds by both palaeobotanists and botanists. The morphology of seeds of the European Mid to Late Tertiary species of Magnolia has been summarized broadly by Kirchheimer (1935, 1936, 1957), who described the morphology and anatomy of the seeds of the family, based on his treatment of the seeds of 25 extant species and the known fossil forms. Mai (1971, 1975) revised the taxonomy of the four most common Magnolia seed species of the European Tertiary and presented a list of their diagnostic characters. In addition, he compiled a working key to the known fossil seeds of the genera from Europe and western Asia. Several Magnolia species have been reported by Dorofeev (1960, 1963,1974), from the Oligocene and Miocene. Three new species of the extinct genus Liriodendroidea from the Cenomanian Turonian were established, according to the close similarity of their seeds to those of the extant Liriodendron (Frumin & Friis, 1999). Tiffney (1977) reported on sclerotesta morphology of 68 species from four extant genera and two new fossil seed species recovered from the Brandon Lignite. His investigation revealed that correlations between species based on their seed characteristics tend to reflect the accepted taxonomic divisions proposed by Dandy (1950). Limited by the seeds involved, Tiffney did not discover polymorphism in the chalazal region morphology, nor reveal the evolutionary trends in morphology, nor indeed the evolutionary relationships within the family Magnoliaceae. Confusion has existed on the classification of Magnoliaceae since Law proposed his system with 15 genera in Nooteboom tended to favour big genera, and reduced the 15, first to seven genera (Cheng & Nooteboom, 1993), and later to three (Nooteboom, 407

2 408 F.-X. XU 2000). The basis for confusion was that morphological characters overlapped among genera and those used for classification were inadequate. Sclerotesta characters are some of the most stable features of Magnoliaceae and need to be studied for classification. A good classification may depend on sclerotesta characters directly or indirectly. This study attempts to recognize morphological distinctions, based on the sclerotesta characters, between the genera within the family, and in many cases, between the species within the genera. MATERIAL AND METHODS Mature seeds of 101 species were obtained, either from specimens collected by Y. W. Law, R. Z. Zhou and F. X. Xu, or from herbarium specimens. Voucher specimens of the plants from which the seeds originated are in the herbaria of the CAS, DS, GH, HITBC, IBSC, K, KUN and YCFI. Sarcotestas were peeled to clean the sclerotesta, with dried seeds that had previously been soaked in warm water. Seeds were coated with gold and observed using a JSM-T300. The terminology mainly follows Tiffney (1977) and Xu & Wu (2000). Species names are listed in Table 1. RESULTS Among the taxa examined, two basic types of chalazal morphology were distinguished: pore type and tube type. Both relate to the passage of the raphal bundle through the sclerotesta to the endosperm. The former is characterized by having a simple pore and the latter by having a more complex structure consisting of a central hollow tube contained within a hole. A detailed description is given below. PORE TYPE Pore round, occasionally elliptic (Talauma). Flat rim, sometimes a little raised (Figs 5, 11). Pore on the top of the chalazal end or the upper ventral face. Taxa with this type of seeds are: Manglietia, Pachylarnax, Magnolia (17 species), Aromadendron, Talauma (eight species), Parakmeria (one species), Kmeria (one species), Elmerrillia, Liriodendron. TUBE TYPE Tube length may vary somewhat, some tube openings enlarged (Fig. 34). Straight orientation in the bottom of the hole, or on the dorsal wall in some American Magnolia species (Fig. 35). All tubes are straight, except in Parakmeria lotungensis, P. yunnanensis and P. kachirachirai where they are bent perpendicular to the longitudinal axes of seeds (Figs 38, 39, 42). Appendages absent or needle-like, plate-like or lamellate, and numerous and dense, encircling the tube to leave only the tube open in Paramichelia baillonii. Hole or deep; rim even or irregularly serrate, ventral rim outline is circular V- or U-shaped. In the genus Magnolia, some North American species have a collar or constriction at the circumference of the seed, near the chalazal end. Taxa with this type of seed are: Manglietiastrum, Magnolia (15 species), Talauma (three species), Parakmeria (four species), Kmeria (one species), Alcimandra, Michelia, Paramichelia and Tsoongiodendron. Six Magnolia species do not possess the typical pore or tube. In these species the pore is surrounded by a few depressions or connected cracks, or is slightly raised. The tube is very short and attached to several lamellae; the hole rim is indistinguishable (Figs 13, 14, 16, 17, 18, 36). Other seed characters found to be useful for identification during the course of this investigation are the orientation of the testa, the presence (or absence) of the sinus on the ventral face and seed shape, size and colour. Most species of Magnolia, Talauam and genera Pachylarnax, Manglietiastrum, Aromadendron and Alcimandra have a smooth seed surface. Depressions are present in Kmeria, Michelia and Paramichelia. The surface of Manglietia seeds possesses slightly raised papillae, rarely smooth. Tsoongiodendron is notably striated at intervals with big tubercles. Liriodedron s rough surface, thin and fragile texture and special seed shape make it markedly different from other Magnoliaceae family members. The sinus, a trace formed by the raphal bundle extending from the chalazal pore or tube to the sclerotesta, is very strongly developed in Manglietia, Aromadendron, Paramichelia and some pore type species of Magnolia but faint or absent in other genera. The shape of the seeds of the Magnoliaceae is generally correlated with the number of seeds per carpel. Those of Manglietia are notably small, cordate in outline but quite angular, resulting from the presence of four or more seeds in the mature carpel (Fig. 69). In contrast, the seeds of Talauma (Figs 57, 60) and Tsoongiodendron (Fig. 67) are particularly large, resulting from the maturation of only one seeds in each carpel. Funicle remains on the micropylar end give the seed of Liriodendron a particularly fish-like outline (Fig. 54). Seed colour is also relatively stable. Seeds of Manglietia, Manglietiastrum, Alcimandra and Paramichelia are mostly black while those of Talauma, Elmerrillia, Tsoongiodendron and Lirodendron are yellow or yellowish. Seed colour of Magnolia and Michelia may vary from yellow or brown to black. The results are summarized in Table 2.

3 SCLEROTESTA MORPHOLOGY 409 Table 1. Species observed and their chalazal form (following the classification system of Law, 1984) Species Provenance Voucher Number (grain) Chalazal form I Manglietia Bl. 1 M. aromatica Dandy Xichou, Yunnan, China Y.W.Law et X.W.Wang pt (IBSC) 2 M. chingii Dandy Renhua, Guangdong, China L.Teng 7227 (IBSC) 6 pt 3 M. conifera Dandy SCBG (introduced from F.X.Xu (IBSC) 2 pt Vietnam) 4 M. dandyi (Gagnep.) Vietnam K.M.Feng 1171 (CAS) 4 pt Dandy 5 M. decidua Q.Y. Zheng Yichun, Jiangxi, China Z.X.Yu (YCFI) 9 pt 6 M. forrestii W.W.Smith Mengla, Yunnan, China C.J.Liao s. n. (IBSC) 4 pt ex Dandy 7 M. garrettii Craib Thailand Y.W.Law (seed) (IBSC) 2 pt 8 M. grandis Hu & Cheng Guangxi, China s.coll., s.n. (IBSC) 8 pt 9 M. hainanensis Dandy Jianfengling, Hainan, R.Z.Zhou 95041(seed) (IBSC) 4 pt China 10 M. insignis Blume SCBG (introduced from F.X.Xu 0104 IBSC) 20 pt Maguan, Yunnan, China) 11 M. maguanica Chang & Maguan, Yunnan, China B.L.Chen (KUN) 2 pt B. L. Chen 12 M. megaphylla Hu Guangxi, China R.Z.Zhou (seed) (IBSC) 8 pt & Cheng 13 M. moto Dandy SCBG (introduced from F.X.Xu (IBSC) 13 pt Beijiang, Guangdong, China) 14 M. pachyphylla H.T.Chang Guangdong, China R.Z.Zhou (seed) (IBSC) 13 pt II Manglietiastrum LawM. Xichou, Yunnan, China Y.W.Law (seed) (IBSC) 5 tt sinicum Y.W.Law III PachylarnaxP. praecalva Kepong, Malaya K.N.Kochummen(K) 1 pt Dandy IV Magnolia L. 1 M. albosericea Chun & C.H. Tsoong Baotin, Hainan, China S.J.Pan 070 (IBSC) 2 pt 2 M. axilliflora (T.B.Chao, T.X. Henan, China Y.W.Law s.n. (seed) (IBSC) 1 tr Zhang & J.T.Gao)T.B.Chao 3 M. axilliflora var. alba Henan, China Y.W.Law s.n. (seed) (IBSC) 8 tr T.B.Chao, Y.H.Ren et J.T.Gao. 4 M. biondii Pampanini Weichen, Gansu, China Z.Y.Zhang 927 (KUN) 5 tr 5 M. campbelli Hook. f. & Lepo, Cuona, Xizang, China G.Y.Xu et al. 853 (KUN) 6 tr Thoms. 6 M. carsonii Dandy ex H.P. Nooteboom Borneo Y.W.Law s.n. (seed) (IBSC) 3 pt 7 M. championi Benth. Garden, China R.Z.Zhou s.n. (seed) (IBSC) 6 pt Shenzhen Fairy Lake Botanical 8 M. coco DC. Luofushan, Guangdong, Y.Jiang 1757 (IBSC) 1 pt China 9 M. cubensis Urb. Eastern Cuba Y.W.Law s.n. (seed) (IBSC) 1 pt 10 M. cylindrica E.H.Wilson Jinggangshan, Jiangxi, unknown (IBSC) 1 tt China 11 M. delavayi Franch. Laoqin, Fuming, Yunnan, China B.Y.Qiu pt

4 410 F.-X. XU Table 1. Continued Species Provenance Voucher Number (grain) Chalazal form 12 M. denudata Desr. SCBG (introduced from R.Z.Zhou s.n. (seed) (IBSC) 40 tt Hangzhou, Zhejiang, China) 13 M. fistulosa Dandy Dapo, Maoming, L.Teng 1774 (KUN) 1 pt Guangdong, China 14 M. globosa Hook. f. Yunnan, China X.T.Cai (IBSC) 4 pt & Thoms. 15 M. grandiflora Linn. SCBG (introduced from R.Z.Zhou s.n. (seed) (IBSC) 22 tt south-east America) 16 M. henryi Dunn Mengla, Yunnan, China Q.T.Zhang (KUN) 3 pt 17 M. hypoleuca Sieb. & Zucc. Japan Y.W.Law s.n. (seed) (IBSC) 6 pt 18 M. iltisiana J.A.Vázquez G. Mexico A.Gentry & E.Jardel tt (DS) 19 M. liliiflora Desr. Eastern Asia R.Z.Zhou s.n. (seed) (IBSC) 1 tt 20 M. macrophylla Michx. USA H.Kearney 609 (CAS) 2 tt 21 M. maingayi King Singapore M.D.Henderson (DS) 1 pt 22 M. officinalis Rehder & Guizhou, China P.X.Tan (IBSC) 6 pt Wilson 23 M. pacifica J.A.Vázquez G. Mexico Y.W.Law s.n. (DS) 2 tt 24 M. paenetalauma Dandy Qingzhou, Guangxi, China H.M.Wu 0027 (IBSC) 2 pt 25 M. panamensis J.A. Mexico Y.W.Law s.n. (GH) 2 tt Vázquez G. & H.H.Iltis 26 M. poasana Dandy Mexico D.E.Breedlove & B.T.Keller 2 tt (CAS) 27 M. pterocarpa Roxb. India John & C.Taylor (CAS) 2 tr 28 M. rostrata W.W.Smith Gaoligong, Gongshan, s.coll (KUN) 2 pt Yunnan, China 29 M. salicifolia Maxim. Kawasiki-machi, Japan A.Azuma & T.Kurosawa tt (IBSC) 30 M. sargentiana Rehder & Tianquan, Sichuan, China X.L.Jiang (IBSC) 2 tr Wilson 31 M. schiedeana Schlecht. Mexico F.A.Ventura 3634 (DS) 1 tt 32 M. sharpii Miranda Mexico A.S.Ton 2319 (DS) 2 tt 33 M. sieboldii K.Koch Wugong, anfu, Jiangxi, J.S.Yue et al (KUN) 24 pt China 34 M. sinensis Stapf Hongya, Sichuan, China S.R.Qiao 1043 (IBSC) 2 pt 35 M. soulangeana Soul. -Bod. Hangzhou Botanical R.Z.Zhou s.n. (IBSC) 2 tt Garden 36 M. sprengeri Pampanini Sichuan, China C.D.Zhang s.n. (IBSC) 4 tt 37 M. tripetala Linn. USA J.Slama 40 (CAS) 15 pt 38 M. uvariifolia Dandy ex Borneo M.Clemens (CAS) 4 pt H.P. Nooteboom 39 M. virginiana Linn. USA Y.W.Law s.n. (GH) 4 tt 40 M. wilsonii Rehder Yunnan, China B.X.Sun 0904 (IBSC) 1 pt V Aromadendron Bl. A. elegans Blume Singapore H.Keng s.n. (IBSC) 3 pt VI Talauma Juss. 1 T. angatensis F.Villar Philippines C.A.Wenzel 2993 (CAS) 6 pt 2 T. candollii Blume Java Island C.S.Sargent s.n. 6 pt 3 T. gigantifolia Miq. Borneo A.D.E.Elmer (GH) 13 pt 4 T. hodgsoni Hook. f. & Tibet, China Y.W.Law (seed) (IBSC) 5 pt Thoms. 5 T. mexicana G.Don Mexico D.E.Breedlove (GH) 3 tt

5 SCLEROTESTA MORPHOLOGY 411 Table 1. Continued Species Provenance Voucher Number (grain) Chalazal form 6 T. obovata Korth Singapore M.R.Hendorson (CAS) 5 pt 7 T. ovata A.St.Hil. Brazil Y.Mexia 5199 (CAS) 2 tt 8 T. persuaveolens ssp. Borneo Y.W.Law (seed) (IBSC) 2 pt rigida (Noot). N. N. Imkhanitskaya 9 T. sambuensis Pittier Panama N.Bristan 1461 (GH) 1 tt 10 T. singapurensis Ridley Malaysia C.Kiah (GH) 2 pt 11 T. villosa Miq. Singapore F.R.I.Kepong (CAS) 3 pt VII Parakmeria Hu et Cheng 1 P. kachirachirai (Kaneh. & Taiwan, China Y.W.Law s.n. (GH) 8 tt Yamam) Y.W.Law 2 P. lotungensis (Chun & C.H. Xingning, Hunan, China M.X.Huang (IBSC) 11 tt Tsoong) Y.W.Law 3 P. nitida (W.W.Sm.) Y.Law Champuton, Yunnan, China F.R.Joseph pt 4 P. omeiensis Cheng Emei, Sichuan, China R.Z.Zhou s.n. (seed)(ibsc) 3 tt 5 P. yunnanensis Hu Xichou, Yunnan China s.coll., s.n. (seed) (IBSC) 24 tt VIII Kmeria Dandy 1 K. septentrionalis Dandy Hechi, Guangxi, China S.N.Gan 1 (IBSC) 26 tt 2 K. duperreana Dandy Thailand A.G.F.Kerr17847 (K) 3 pt IX Alcimandra Dandy A. cathcartii Dandy Wenshan, Yunnan, China R.Z.Zhou 29 (IBSC) 20 tt X Elmerrillia Dandy 1 E. ovalis Dandy Moluccas, Indonesia Y.W.Law (seed) (IBSC) 12 pt 2 E. tsiampacca (L.) Dandy Philippines A.N.Miller 2341 (DS) 25 pt XI Michelia L. 1 M. alba DC. SCBG (introduced from Y.W.Law (seed) (IBSC) 2 tt Malaysia) 2 M. balansae Dandy SCBG (introduced from F.X.Xu (IBSC) 4 tt Hainan, China) 3 M. cavaleriei Finet & Yuanyang, Yunnan, China S.C.He (IBSC) 2 tt Gagnep. 4 M. champaca Linn. SCBG (introduced from F.X.Xu (IBSC) 21 tt Longzhou, Guangxi, China) 5 M. chapensis Dandy Huaiji, Guangdong, China Y.Q Cheng (IBSC) 10 tt 6 M. compressa (Maxim.)Sarg. SCBG (introduced from Taiwan, China) Y.H.Law95024 (seed) (IBSC) 3 tt 7 M. crassipes Y.W.Law SCBG (introduced from F.X.Xu (IBSC) 8 tt Guangxi, China) 8 M. doltsopa Buch.-Ham. Yaojia pin, Lushui, Yunnan, S.G.Wu 8490 (HITBC) 4 tt ex DC. China 9 M. floribunda Finet & SCBG(introduced from F.X.Xu (IBSC) 12 tt Gagnep. Xinning, Hunan, China) 10 M. foveolata Merrill ex Dandy SCBG(introduced from Ruyuan, Guangdong, China) F.X.Xu (IBSC) 11 tt 11 M. guangxiensis Y.W.Law & R.Z.Zhou SCBG (introduced from Miaoershan, Guangxi, China) F.X.Xu (IBSC) 15 tt 12 M. hedyosperma Y.W.Law Manka, Jinghong, Yunnan, Y.H.Li & P.H.Yu tt China (HITBC) 13 M. longipetiolata C.Y. Wu ex Y.W.Law & Y.F.Wu Hunan, China R.Z.Zhou (seed) (IBSC) 4 tt

6 412 F.-X. XU Table 1. Continued Species Provenance Voucher Number (grain) Chalazal form 14 M. longistamina Y.W.Law SCBG (introduced from F.X.Xu (IBSC) 1 tt Guangdong, China) 15 M. macclurei Dandy SCBG (introduced from F.X.Xu (IBSC) 1 tt Shiwandashan, Guangxi, China) 16 M. maudiae Dunn SCBG (introduced from F.X.Xu (IBSC) 23 tt Conghua, Guangdong, China) 17 M. montana Blume Malaysia, India Y.W.Law (seed) (IBSC) 2 tt 18 M. skinneriana Dunn SCBG (introduced from F.X.Xu (IBSC) 6 tt Conghua, Guangdong, China) 19 M. velutina DC. Wuyishan, Fujian, China Y.W.Law (seed) (IBSC) 1 tt 20 M. wilsonii Finet & Gagnep. Emei, Sichuan, China R.Z.Zhou (seed) (IBSC) 1 tt 21 M. yunnanensis Franch. ex SCBG (introduced from F.X.Xu (IBSC) 50 tt Finet & Gagnep. Kunming, Yunnan, China) XII Paramichelia Hu P. baillonii (Pierre) Hu Mengla, Yunan, China H.Wang (seed) (IBSC) 80 tt XIII Tsoongiodendron Chun T. odorum Chun Gaoyao, Guangdong, China C.Huang (IBSC) 27 tt XIV Liriodendron L. 1 L. chinense Sargent SCBG (introduced from F.X.Xu (IBSC) 14 pt south-east America) 2 L. tulipifera Linn. SCBG (introduced from Guilin, Guangxi, China) F.X.Xu (IBSC) 4 pt Abbreviations CAS = Herbarium, Botany Department, California Academy of Sciences; DS = Dudley Herbarium of Stanford University, Botany Department, California Academy of Sciences; GH = Harvard University Herbaria; HITBC = Herbarium of Yunnan Institute of Tropical Botany, Academia Sinica; IBSC = Herbarium, Taxonomy Department, South China Institute of Botany, Academia Sinica; K = the Herbarium, Royal Botanic Gardens, Kew Richmond, England, Great Britain; KUN = Herbarium of Kunming Institute of Botany, Academia Sinica; SCBG = South China Botanical Garden, South China Institute of Botany, the Chinese Academy of Sciences, China; YCFI = Yichun Forestry Institute; pt = pore type; tr = transitional type; tt = tube type. Figures Chalazal form (SEM) in Magnoliaceae. Scale bars = 400mm. Figs 1-12, 15. Pore type. Fig. 1 Manglietia aromatica. Fig. 2. Manglietia decidua. Fig. 3. Manglietia garrettii: the pore on the end of the ventral face. Fig. 4. Aromadendron elegans. Fig. 5. Parakmeria nitida: the pore raised a little, a scar under the pore. Fig. 6. Liriodendron chinense. Fig. 7. Kmeria duperreana. Fig. 8. Talauma gigantifolia: the pore on the upper ventral face. Fig. 9. Talauma singapurensis: elliptic pore. Fig. 10. Elmerrillia tsiampacca. Fig. 11. Pachylarnax praecalva: the pore raised a little. Fig. 12. Talauma hodgsoni: elliptic pore. Fig. 15. Talauma obovata. Figs 13,14,16,17,18. Transitional type. Fig. 13. Magnolia axilliflora: pore surrounded by several depressions. Fig. 14. Magnolia axilliflora var. alba: more depressions. Fig. 16. Magnolia pterocarpa: the pore raised, connected with cracks. Fig. 17. Magnolia biondii: the tube very short, attached to lamellar. Fig. 18. Magnolia campbelli: hole rim undistinguished. The arrows show the pore (Figs 4,13,14,16) or the lamellae (Figs 17,18).

7 SCLEROTESTA MORPHOLOGY 413

8 414 F.-X. XU Figures Scale bars = 400mm. Figs 19 23, 26 27, 29 30, Tube type. Figs 24,25,28,31. Pore type. Fig. 19. Tsoongiodendron odorum. Fig. 20. Magnolia poasana. Fig. 21. Alcimandra cathcartii. Fig. 22. Magnolia cylindrica. Fig. 23. Magnolia macrophylla. Fig. 24. Magnolia maingayi: elliptic pore. Fig. 25. Magnolia officinalis. Fig. 26. Magnolia pacifica. Fig. 27. Magnolia salicifolia. Fig. 28. Magnolia wilsonii. Fig. 29. Magnolia virginiana. Fig. 30. Magnolia sprengeri: showing hole and lamellar. Fig. 31. Magnolia tripetala: the pore on the end of the ventral face. Fig. 32. Magnolia liliiflora. Fig. 33. Manglietiastrum sinicum. Fig. 34. Magnolia grandiflora. Fig. 35. Magnolia sharpii: the tube on the dorsal wall. Fig. 36. Magnolia sargentiana: transitional type, the tube distinguished, the hole rim unclear. The arrow shows the lamella (Figs 19, 30). Figs 20, 23, 26, 29, 34, 35 show the V-shaped ventral rim and the collar in American species.

9 SCLEROTESTA MORPHOLOGY 415 Figures Scale bars = 400 mm. Tube type. Fig. 37. Parakmeria omeiensis. Fig. 38. Parakmeria yunnanensis: tube bent to the ventral face. Fig. 39. Parakmeria lotungensis: tube bent to the ventral face. Fig. 40. Michelia skinnerriana. Fig. 41. Michelia wilsonii: the tube is very short with lamellar attached to the hole. Fig. 42. Parakmeria kachirachirai: tube bent at the up of the tube. Fig. 43. Michelia champaca: the tube is very short with lobes. Fig. 44. Michelia longipetiolata. Fig. 45. Michelia crassipes. Fig. 46. Michelia alba: corn tube. Fig. 47. Michelia velutina: very short tube. Fig. 48. Kmeria septentrionalis: the tube on the base of the dorsal wall. Fig. 49. Michelia cavaleriei. Fig. 50. Talauma ovata. Fig. 51. Talauma sambuensis. Fig. 52. Paramichelia baillonii. The arrows show the tube (Fig. 52) or the lamella (Figs 49, 50).

10 416 F.-X. XU 53 v Figures Shape of magnoliaceous seeds. Scale bar = 10 mm. v = ventral face; d = dorsal face. Fig. 53. Michelia champaca. Fig. 54. Liriodendron chinense: fish-like shape. Fig. 55. Kmeria duperreana. Fig. 56. Michelia maudiae. Fig. 57. Talauma persuaveolens var. rigida: pyramid shape. Fig. 58. Pachylarnax praecalva: bean-like shape. Fig. 59. Kmeria septentrionalis. Fig. 60. Talauma sambuensis. Fig. 61. Paramichelia baillonii: striated and depressed surface. Fig. 62. Magnolia pacifica: showing collar and Y-lined scar. DISCUSSION 1 The chalazal region morphology is unique and has been found only in Magnoliaceae. It is not present in the families related to Magnoliaceae, such as Illiciaceae, Schisandraceae and Winteraceae, that the author studied previously (Xu, 2000a). The morphology is also stable in this family. Seeds show one 59 type or the other. Most genera have just one chalazal form (pore or tube type) except for four that have two. The results show no intraspecific variation in chalazal form within a simple plant, and chalazal morphology does not vary between different collections of the same species, and there is very little in the size and testa characters of the seed itself in a species. 60

11 SCLEROTESTA MORPHOLOGY Figures Fig. 63. Parakmeria yunnanensis. Fig. 64. Magnolia liliiflora. Fig. 65. Alcimandra cathcartii: smooth surface. Fig. 66. Magnolia hypoleuca: deep sinus. Fig. 67. Tsoongiodendron odorum: striated interval with tubercles surface. Fig. 68. Aromadendron elegans: broad and deep sinus. Fig. 69. Manglietia dandyi: papillary surface. Fig. 70. Elmerrillia tsiampacca: depressed surface. 2 Genera Manglietia, Pachylarnax, Aromadendron, Elmerrillia and Liriodendron are of pore type, Manglietiastrum, Alcimandra, Michelia, Paramichelia and Tsoongiodendron are of tube type. Talauma is dominantly of pore type, but Parakmeria is dominantly tube type. Two species of Kmeria have one of pore type and the other tube type. In Magnolia, the number of species with pore and tube types are similar. The seeds of the Asian and American species may be distinguished by some characters. American species have more tube type seeds, with a deep hole and possess a collar or constriction around the circumference of the seed near the chalazal end. The ventral rim is always V-shaped, linked with the sinus leaves by a Y-lined scar on the smooth testa (Fig. 62). Moreover, the seeds are usually yellow in colour. In contrast, the Asian species have more pore type seeds than tube type. Those of the tube type have a short tube, hole and are thick to the rim hole, an appendage is always found in the hole or attached to the tube, and the seeds are often black in colour

12 418 F.-X. XU pt tt pt both both pt both tt tt pt tt tt tt pt Mang Manli Pachy Mag Tala Dugan Aro Pake Kme Alci Elme Miche Pami Tsoon Liri Elmerrilliinae Micheliinae Manglietiinae Magnoliinae Magnolieae Magnolioideae Magnoliaceae Michelieae Liriodendroideae Figure 71. Distribution of the pore type and the tube type of the chalazal region in the genera of the Magnoliaceae. Abbreviations: pt = pore type; tt = tube type; both = pore type and tube type; Mang = Manglietia; Manli = Manglietiastrum; Pachy = Pachylarnax; Mag = Magnolia; Tala = Talauma; Dugan = Dugandiodendron; Aro = Aromadendron; Pake = Parakmeria; Kme = Kmeria; Alci = Alcimandra; Elme = Elmerrillia; Miche = Michelia; Pami = Paramichelia; Tsoon = Tsoongiodendron; Liri = Liriodendron. Table 2. Sclerotesta characters of observed species Species Raphal sinus Surface character Colour Shape Size (mm) (width length) 1 Manglietia aromatica broad and deep papillary black flattened cordate 4 5 M. chingii papillary brown cordate 6 6 M. confera broad and deep papillary yellow bean-like, cordate (5~7) (4~5) M. dandyi broad and deep papillary black cordate (4~7) (5~6) M. decidua broad smooth black cordate (7~9) (4~5) M. forrestii broad and deep papillary 1 black, 3 yellow cordate (4~6) (6~7) M. garrettii papillary yellow cordate 6 6 M. grandis broad and deep striated brown cordate (6~8) 9 M. hainanensis broad and deep papillary black cordate, 5 6 obtriangular M. insignis broad and deep striated and black cordate, (6~10) (6~7) depressed obtriangular M. maguanica broad and deep papillary yellow cordate 6 7 M. megaphylla broad and deep papillary black cordate 6 7 M. moto broad and deep papillary black cordate, bean-like (5~8) (3~6) M. pachyphylla papillary yellow, black cordate (5~7) 5 2 Manglietiastrum absent smooth black transversely (9~12) (6~7) sinicum obovoid 3 Pachylarnax absent smooth brown bean-like 8 5 praecalva 4 Aromadendron broad and deep smooth brown cordate (8~9) (6~8) elegans 5 Magnolia albosericea thin and smooth brown obtriangular 8 9 M. axilliflora broad and smooth brown cordate 11 8 M. axilliflora var. alba broad and smooth black cordate 11 8

13 SCLEROTESTA MORPHOLOGY 419 Table 2. Continued Species Raphal sinus Surface character Colour Shape Size (mm) (width length) M. biondii broad and smooth black cordate 8 9 M. campbelli absent smooth light yellow cordate 8 11 M. carsonii broad and deep smooth 1 brown, 1 yellow cordate (6~8) 8 M. championi smooth brown bean-like 9 8 M. coco absent smooth brownish red obovoid 7 9 M. cubensis absent smooth black obtriangular 8 8 M. cylindrica broad and smooth black cordate 9 8 M. delavayi absent striated light yellow cordate 5 8 M. denudata broad and smooth black cordate (8~11) (7~10) M. fistulosa absent smooth light brown cordate 9 8 M. globosa absent smooth black cordate 8 8 M. grandiflora smooth yellow obovoid 7 9 M. henryi broad and short depressed yellow cordate 9 9 M. hypoleuca broad and deep smooth 2 yellow, 4 black cordate (7~10) 10 M. iltisiana smooth yellow cordate 7 10 M. liliiflora faint smooth brownish red cordate 8 8 M. macrophylla smooth brown obovoid (7~8) (10~11) M. maingayi absent smooth yellow cordate 8 7 M. officinalis broad and deep smooth brown obtriangularobvoid (7~10) (8~13) M. pacifica smooth yellow cordate (6~7) 8 M. paenetalauma absent smooth 1 yellow, 1 brown obovoid (11~19) (6~7) M. panamensis absent smooth yellow flattened cordate 6 7 M. poasana faint smooth yellow obtriangular 7 8 M. pterocarpa thin and deep striated brown obovoid 8 9 M. rostrata faint smooth black cordate 5 7 M. salicifolia absent smooth black cordate 6 6 M. sargentiana absent smooth yellow obovoid (7~10) 9 M. schiedeana smooth yellow cordate 6 6 M. sharpii faint smooth yellow obovoid 7 11 M. sieboldii absent striated black cordate 7 8 M. sinensis faint smooth brown cordate (6~8) 5 M. soulangeana broad and smooth brownish red obovoid 9 8 M. sprengeri broad and smooth black bean-like (8~10) (7~10) M. tripetala wide and deep striated black cordate (7~9) 8 M. uvarifolia wide and smooth yellow cordate (7~10) 9 M. virginiana smooth yellow cordate (5~7) 7 M. wilsonii absent smooth black obovoid Talauma angatensis thin and striated yellow bean-like (9~13) (10~13) T. candollei absent striated brown pyramid 10 7 T. gigantifolia faint striated yellow cordate (10~14) (14~10) T. hodgsoni absent smooth yellow cordate 8 9 T. obvata absent striated yellow obtriangular T. persuaveolens absent smooth yellow pyramid (10~12) (8~10)

14 420 F.-X. XU Table 2. Continued Species Raphal sinus Surface character Colour Shape Size (mm) (width length) T. singapurensis absent smooth yellow obtriangular 9 10 T. villosa thin and depressed yellow bean-like 12 5 T. mexicana faint smooth brown obtriangular (9~10) (10~11) T. ovata faint striated brown cordate 7 11 T. sambuensis broad, short striated light yellow cordate 9 10 and 7 Parakmeria nitida faint smooth brown obtriangular (8~10) (6~8) P. kachirachirai absent smooth yellow flattened cordate (6~8) (6~8) P. lotungensisi faint smooth brown bean-like (4~8) (5~11) P. omeiensis absent smooth brown bean-like (10~14) (6~7) P. yunnanensis absent smooth brown cordate (10~13) 7 8 Kmeria absent depressed brown cordate 10 6 septentrionalis K. duperreana absent depressed 1 brown, 1 yellow cordate Alcimandra absent smooth black cordate 8 7 carthcartii 10 Elmerrillia ovalis faint depressed black, yellow bean-like 5 (4~5) E. tsiampacca faint depressed black, yellow bean-like (5~6) (4~5) 11 Michelia alba absent depressed 1 black, 1 yellow cordate 10 8 M. balansae absent depressed yellow obovoid 11 8 M. cavaleriei absent smooth black cordate 6 7 M. champaca absent depressed brown obovoid 5 7 (present occasionally) M. chapensis absent depressed brown obovoid (9~12) (8~9) M. compressa absent striated and brown cordate 5 6 depressed M. crassipes absent warty-rough yellow cordate 8 8 M. doltsopa absent depressed yellow bean-like 9 9 M. floribunda absent warty-rough yellow cordate 10 8 M. foveolata absent depressed yellow cordate 8 6 M. guangxiensis absent striated yellow cordate (9~10) (8~9) M. hedyosperma absent striated yellow cordate 8 9 M. longipetiolata absent depressed 2 yellow, 2 black bean-like (5~10) (6~7) M. longistamina absent depressed brown obovoid 5 9 M. macclurei var. absent striated brown cordate 7 6 sublanea M. maudiae absent depressed brown obovoid 8 7 M. montana absent depressed black cordate (8~10) 8 M. skinneriana absent depressed brown cordate 8 6 M. velutina absent depressed brown cordate 7 5 M. wilsonii absent depressed black cordate 7 7 M. yunnanensis absent striated black cordate Paramichelia deep striated and black obovoid (5~6) (8~9) baillonii depressed 13 Tsoongiodendron absent striated and yellow obtriangular (7~9) (12~15) odorum tuberclate obovoid 14 Liridendron faint warty-rough yellow-brown fish-like 3 6 chinense L. tulipifera faint warty-rough yellow-brown fish-like 2 4

15 SCLEROTESTA MORPHOLOGY 421 Table 3. Sections of Magnolia and the chalazal form of the species examined (based on Dandy in Treseder, 1978) Subgenus Section Species Chalazal form I Magnolia Sect 1. Gwillimia (15) M. albosericea pt M. championi pt M. coco pt M. delavayi pt M. fistulosa pt M. henryi pt M. paenetalauma pt Sect 2. Lirianthe (1) M. pterocarpa tr Sect 3. Rhytidospermum (9) M. hypoleuca pt M. macrophylla tt M. officinalis pt M. rostrata pt M. tripetala pt Sect 4. Magnolia (1) M. virginiana tt Sect 5. Oyama (4) M. globosa pt M. sinensis pt M. sieboldii pt M. wilsonii pt Sect 6. Theorhodon (18) M. cubensis pt M. grandiflora tt M. iltisiana tt M. pacifica tt M. panamensis tt M. poasana tt M. schiedeana tt M. sharpii tt Sect 7. Gynopodium (4) M. kachirachirai tt M. nitida pt M. lotungensis tt Sect 8. Maingola (7) M. carsonii pt M. uvarifolia pt M. maingayi pt II Yulania Sect 9. Yulania (9) M. campbelli tr M. denudata tt M. sargentiana tr M. sprengeri tt Sect 10. Buergeria (5) M. biondii tr M. cylindrica tt M. salicifolia tt Sect 11. Tulipastrum (2) M. liliiflora tt Notes: pt = pore type, tr = transitional type, tt = tube type; The figure is the species number in each section; M. soulangeana (hybrid), M. axilliflora and M. axilliflora var. alba are not in the table because sections are unknown. 3 The pore type is primitive and the tube type advanced. Primitive taxa according to the system of Law (1984) have pore type seeds, while more advanced taxa have tube type seeds. For example, species of Elmerrilliinae (with only one genus Elmerrillia) are considered to be more primitive than Micheliinae, which includes Michelia, Paramichelia and Tsoongiodendron. The seeds of the former are of the pore type while those of the latter are all tube type. Furthermore, all species examined in

16 422 F.-X. XU Table 4. Key to magnoliaceous genera (species) based on seed characters 1 Pore type 2 1 Tube type 11 2 Sinus wide and deep 3 2 Sinus and absent 6 3 Sclerotesta smooth 4 3 Sclerotesta rough 5 4 Seeds (8 9) (6 8)mm Aromadendron 4 Seeds (7 10) 10mm Magnolia hypoleuca, M. officinalis, M. tripetala 5 Seeds plat-cordate or triangular Manglietia 5 Seeds fish-like Liriodendron 6 Sclerotesta depressed 7 6 Sclerotesta smooth or striated 8 7 Seeds 10 7mm Kmeria duperreana 7 Seeds 5 4mm Elmerrillia 8 Pore rim raised 9 8 Pore rim never raised 10 9 Seeds cordate, 9 8mm Parakmeria nitida 9 Seeds bean-like, 8 5mm Pachylarnax 10 Seeds yellow, pyramid Talauma 10 Seeds black, cordate Magnolia 11 Tube bent at the base or the upper part Parakmeria 11 Tube straight, never bent Sclerotesta tuberclate Tsoongiodendron 12 Sclerotesta non-tuberclate Sclerotesta depressed Sclerotesta smooth or striated Tube parallel to the longitudinal axes of seeds Michelia 14 Tube slin to the longitudinal axes of seeds Kmeria septentrionalis 15 Tube short, hole, with rim undistinguishable Manglietiastrum 15 Tube long, hole large and deep, with distinct rim Appendages attached to the hole or the tube No appendages attached to the hole or the tube Appendage lamellae numerous and dense Paramichelia 17 Appendage lamellae one or two Seeds yellow, pyramid Talauma 18 Seeds black, cordate Magnolia (Asian species) 19 Seeds yellow, with collar in the chalazal end Magnolia (American species) 19 Seeds black, without collar in the chalazal end Alcimandra Manglietia, which is considered as the most primitive taxon in Magnoliaceae, are of pore type, including the only deciduous species found; M. deciduas (Zheng, 1995). The members of the subgenus Magnolia are evergreen and have more primitive characters than those of the deciduous subgenus Yulania. The seeds of subgenus Magnolia are mostly of the pore type, except in section 4 and section 6 (based on Dandy in Treseder (1978)) which are tube type (Table 3). The latter are distributed mainly in America. Three species of section Gynopodium also have tube type seeds, but have been treated as a separate genus in Law s system (1984). Seeds of subgenus Yulania are mostly of the tube type except for several transitional types with a very short tube. From this study, it appears that the pore type is more primitive than the tube type. If the pore becomes raised, the surrounding depression may be enlarged and deepened to become the hole and subsequently, the pore becomes the tube. 4 The sinus seems to be a primitive character. It appears in primitive taxa, such as Manglietia and Aromadendron, where it is very strongly developed. In Magnolia and Talauma, species with a sinus are often of the pore type. 5 It is worth noting that the systematic status of some genera may be determined on the chalazal form.

17 SCLEROTESTA MORPHOLOGY 423 Manglietia sinicum was treated as a separate genus by Law (1979) because its stipules fall without leaving a scar around the twig, the carpels become completely connate after fertilization, and mature carpels dehisce along the ventral suture towards the apex and gynopodium. These characteristics are all different from other species in Manglietia. Nooteboom reduced it to Magnolia as subgenus Manglietiastrum at first (1985) and then considered it a species of Manglietia (Cheng & Nooteboom, 1993). The study indicates that five seeds of Manglietiastrum are tube type, which is obviously different from those of Manglietia, in which all species are of pore type. In addition, seeds of Manglietiastrum lack a sinus and have smooth testa while those of Manglietia are very different. The seed characters clearly support the separation of Manglietiastrum. Liriodendron is very distinct in Magnoliaceae, since its leaves are 2 10 lobed, the apex truncate or widely emarginate, and stipules are always free from the petiole. Anthers are extrorse, and the fruit is caducous. The testa adheres to the end of the endocarp. Pollen sculpturing is coarsely rugulose and shows other specialized and advanced characters. The left funicle on the micropyle give the seed a fish-like appearance, a different shape from any other family members. The chalazal pore type of Liriodendron is a very important feature in identification of fossil seeds; it is highly conservative and stable. Liriodendron fits naturally in this family. However it seems to have separated very early and developed into a distinct group which accords with other research findings (Baranova & Jeffrey, 2000; Xu, 2000b). Paramichelia is characterized by the tube surrounded by encompassing lamellae and Tsoongiodendron by its large size, and warty-rough and striated testa, that is very different from that of Michelia. From seed morphology, it is unreasonable to consider Paramichelia and Tsoongiodendron as congeneric with Michelia as Nooteboom suggested (1985). That Paramichelia is closer to Michelia is undoubtedly supported by testa features, seed size and colour. Subgenus Yulania was recently proposed as a distinct genus. Studies show that seed characters of subgenus Yulania are very similar to those of subgenus Magnolia except that species with the tube type predominate. Subgenus Yulania is definitely more advanced than subgenus Magnolia. From the data presented in the study, it may be concluded that seed characters are very useful for the identification of magnoliaceous genera, and even species (Table 4). ACKNOWLEDGEMENTS The author received assistance from many individuals during the course of the work and I express my appreciation to all. I am particularly grateful to Professors Yuh-Wu Law, Qi-Gen Wu, Ren-Zhang Zhou and Qing- Wen Zeng for seed collections, to Ms Xiao-Ying Hu for helping with SEM operation and to Ms Yun-Xiao Liu for making the drawings. The project was supported by the National Science Foundation of China (grant number ) and the National Science Foundation of Guangdong province, China (grant number ). REFERENCES Baranova MA, Jeffrey C Stomatographical features in the systematics of the Magnoliaceae. Botanical Journal 85 (6): Cheng BL, Nooteboom HP Notes on Magnoliaceae III, the Magnoliaceae of China. Annals of the Missouri Botanical Garden 80 (4): Dandy JE A survey of the genus Magnolia together with Manglietia and Michelia. In: The Royal Horticultural Society, ed. Camellias and Magnolias. London: Spottiswoods, Ballantyne and Co Ltd, Dorofeev PI The Oligocene flora from the Dunaevsky ravine on the Tym River (Western Siberia). Doklady Akademiia Nauk SSSR 132: (In Russian). Dorofeev PI Tertiary Floras of western Siberia. Leningrad: Izdat. Akademii Nauk SSSR, Botanicheskii Institut V L Komarov. (In Russian). Dorofeev PI Species established according to seeds. In: Takhtajan A, ed. Magnoliophyta Fossilia U.R.S.S. Leningrad: Izdat. Nauka (In Russian). Frumin S, Friis EM Magnoliid reproductive organs from the Cenomanian-Turonian of north-western Kazakhstan. Magnoliaceae and Illiciaceae. Plant Systematics and Evolution 216: Kirchheimer F Bau und botanische Zugehörigkeit von Pflanzenresten aus deutschen Braunkohlen. Botanische Jahrbucher 67: Kirchheimer F Beiträge zur Kenntnis der Tertiärflora. Früchte und Samen aus dem deutschen Tertiär. Palaeontographica Abteilung B 82: Kirchheimer F Die Laubgewächse der Braunkohlenzeit. Halle (Saale): Wilhelm Knapp. Law YW A new genus of Magnoliaceae from China. Acta Phytotaxonomica Sinica 17 (4): Law YW A preliminary study on the taxonomy of the family Magnoliaceae. Acta Phytotaxonomica Sinica 22 (2): Mai DH Fossile Fund von Manglietia Blume (Magnoliaceae). Feddes Repert 82: Mai DH Beitrage zur Bestimmung und Nomenklatur Fossiler Magnolien. Feddes Repert 86: Nooteboom HP Notes on Magnoliaceae I. Blumea 31 (1): Nooteboom HP Different looks at the classification of the Magnoliaceae. In: Liu YH, Fan HM, Chen ZY, Wu QG, Zeng QW, eds. Proceedings of the international symposium of the family Magnoliaceae. Beijing: Science Press, Tiffney BH Fruits and seeds of the Brandon Lignite:

18 424 F.-X. XU Magnoliaceae. Botanical Journal of the Linnean Society 75: Treseder NG Magnolias. London: Faber and Faber. Xu FX. 2000a. Morphology of chalazal region on endotesta in the seeds of Magnoliaceae and those of related families. Subtropical Plant Research Communications 29 (2): Xu FX. 2000b. A cladistic analysis of Magnoliaceae. Journal of Tropical and Subtropical Botany 8 (3): Xu FX, Wu QG Morphology of the chalazal region on the endotesta of seeds in genera Magnolia, Parakmeria and Kmeria. In: Liu YH, Fan HM, Chen ZY, Wu QG, Zeng QW, eds. Proceedings of the International Symposium of the Family Magnoliaceae. Beijing: Science Press, Zheng QY A new specific name of Manglietia. Acta Phytotaxonomica Sinica 33: 180.