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Volume 90 Number 4 2003 Annals of the Missouri Botanical Garden

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Volume 90 Annals Number 4 of the 2003 Missouri Botanical Garden A REVISION OF THE Yelin Huang,2 Peter W. Fritsch,3 and 2 IMBRICATE GROUP OF Suhua Shi STYRAX SERIES CYRTA (STYRACACEAE) IN ASIA1 ABSTRACT Several taxonomic treatments of Styrax (Styracaceae) exist in regional ¯oras of Asia, but the Asian species of the genus have not been comprehensively revised since 1907. To help rectify this, we conducted a taxonomic revision of the Asian species of Styrax series Cyrta with imbricate corolla aestivation. Our revision comprises 17 species with a combined distribution from Japan south to Sumatra and west to Nepal. The circumscriptions of the heretofore poorly de®ned species S. hookeri and S. serrulatus are clari®ed. Styrax agrestis var. curvirostratus is elevated to the species level, and lectotypes are selected for S. duclouxii, S. ¯oribundus, S. hemsleyanus, S. hookeri, S. hookeri var. yunnanensis, S. hypoglaucus, S. japonicus, S. limprichtii, S. macranthus, S. obassia, S. perkinsiae, S. serrulatus var. latifolius, S. shiraianus, S. supaii, and S. wilsonii. Keys, descriptions, and distribution maps are provided for all species. Key words: eastern Asia, Styracaceae, Styrax, Styrax series Cyrta. Styrax L. comprises about 130 species of trees ern Argentina and Uruguay (Fritsch, 1999, 2001). and shrubs distributed in eastern and southeastern Styrax is by far the largest and most widespread of Asia, the New World, and the Mediterranean region the 11 genera in the Styracaceae sensu Fritsch et (Fritsch, 1999). The range of this genus is typical al. (2001) and Fritsch (in press a). Characters of many plant groups distributed among the refugia unique to Styrax in relation to the family include a of Tertiary mixed-mesophytic forests in the North- stamen tube attached high (vs. low) on the corolla, ern Hemisphere, except that it also includes a large the presence (vs. absence) of placental obturators, Neotropical component that extends south to north- bitegmic (vs. unitegmic) ovules, and an indu- 1 We thank the curators of the herbaria listed in the Materials and Methods section, who kindly made specimens available. We are especially grateful to Bruce Bartholomew for help with the collection database and ArcView software, Juan Ochoa for help with distribution maps, and Meg Stalcup for illustrations. We also thank Kanchi Gandhi and Hideaki Ohba for nomenclatural assistance, and Walter Judd, Jun Wen, and an anonymous reviewer for helpful com- ments on the manuscript. This work was supported in part by National Natural Science Foundation of China grants 30230030 and 39825104 to S. Shi. We thank the Lakeside Foundation of the California Academy of Sciences for providing the funds for Y. Huang to spend nine months in the U.S.A for this study. 2 State Key Laboratory for Biocontrol, School of Life Sciences, Sun Yatsen University, Guangzhou 510275, China. [email protected] (Y. Huang); [email protected] (S. Shi). 3 Department of Botany, California Academy of Sciences, San Francisco, California 94118-4599, U.S.A. [email protected]. ANN.MISSOURI BOT.GARD. 90: 491±553. 2003. 492 Annals of the Missouri Botanical Garden rate (vs. thin) seed coat; these have been identi®ed deciduous section Styrax (about 33 species) was as putative synapomorphies for the genus (Fritsch, supported by the presence of young shoots with 1999; Fritsch et al., 2001). The combination of the scattered stalked stellate trichomes distinct from following characters also serves to delimit Styrax the rest of the vestiture patterns (vs. without stalked from other genera of Styracaceae: absence of bud trichomes unless accompanied by a dense tomen- scales, presence of pseudoterminal fertile shoots tum consisting of trichomes of the same general (except in S. macrocarpus W. C. Cheng; presumably type) and membranaceous (vs. subcoriaceous) co- a reversal), a short hypanthium, unarticulated ped- rolla lobes, whereas the clade corresponding to sec- icels, glossy stamen ®lament trichomes that are cir- tion Valvatae GuÈrke (about 97 species) was sup- cular in cross section, a 3-carpellate ovary, the ported by valvate (vs. imbricate or subvalvate) presence of mesocarp, and a seed-to-carpel ratio # corolla aestivation, the evergreen (vs. deciduous) 1 (Fritsch et al., 2001; Fritsch, in press a). Like condition, sides of the corolla straight (vs. convex) other Styracaceae, Styrax has a vestiture of stellate in bud, and concave (vs. planar) stamen ®laments. trichomes (in some cases modi®ed to peltate scales The delimitation of these two species groups cor- or rarely simple trichomes), generally twice the responds roughly to a geographic distribution in number of stamens as petals, and introrsely dehis- warm-temperate versus humid-tropical regions, re- cent anthers with a large, linear connective (Fritsch spectively. Within section Styrax, the clade corre- et al., 2001; Fritsch, in press a). sponding to series Styrax (3 species, western North America, Mediterranean region) was supported by TAXONOMIC HISTORY AND PRESENT OBJECTIVES strictly pseudoterminal (vs. pseudoterminal and lat- eral) in¯orescences, whereas that corresponding to In the most recent worldwide monograph of the series Cyrta (Lour.) P. W. Fritsch (about 30 species, genus (Perkins, 1907), Styrax was divided into sec- eastern and southeastern Asia, southern North tion Styrax, with 16- to 24-ovulate gynoecia (most America) was supported by glandular-serrate (vs. of the genus) and section Foveolaria (Ruiz & Pav.) entire) leaf margins. Perkins, with 3- to 5-ovulate gynoecia (2 Neotrop- The character states of corolla aestivation delim- ical species). Section Styrax was in turn divided ited in the morphological analysis re¯ected the dis- into series Styrax (5 series Imbricatae Perkins, in- tinction made previously (Perkins, 1907; Steenis, valid name) and series Valvatae (GuÈrke) Perkins, 1932) between a truly valvate type of corolla aes- each de®ned, as the names suggest, on the basis of tivation and the subvalvate type. The results of corolla aestivation. Despite the use of aestivation Fritsch (1999) demonstrated that valvate aestiva- type for infrageneric delimitation, Perkins (1907) tion as de®ned by Perkins has evolved at least acknowledged that some species of Styrax placed twice in Styrax, once in the most recent common in series Valvatae are occasionally slightly imbri- ancestor of the evergreen species and once (as the cate (5 ``subvalvate''), whereby the edges of the subvalvate condition) in the deciduous species. corolla lobes are contiguous but oblique in cross Therefore, according to Fritsch's revision, valvate section, with a mixed condition of valvate and sub- aestivation is possessed by all members of section valvate aestivation sometimes occurring within one Valvatae, imbricate aestivation is possessed by all and the same ¯ower. On this basis, Steenis (1932), members of series Styrax and some members of se- in a revision of the Malesian species of Styrax, did ries Cyrta, and the remaining members of series not recognize either series of Perkins and placed Cyrta possess the subvalvate type. The morpholog- several imbricate-¯owered species of series Styrax ical analysis of Fritsch (1999) supported the idea (S. subpaniculatus Jungh. & de Vriese, S. porteri- of Hwang (1999) that imbricate aestivation is the anus G. Don, and S. subdenticulatus Miq.) under S. primitive state in Styrax. serrulatus Roxb., a species with otherwise valvate A molecular phylogenetic analysis of Styrax to subvalvate aestivation. based on DNA sequences from the internal tran- Fritsch (1999) conducted a morphological phy- scribed spacer (ITS) region of nuclear ribosomal logenetic analysis of Styrax and revised the infra- DNA, both separately and in combination with mor- generic classi®cation of the genus based on the re- phology, provided strong support for the series clas- sults. In addition to corolla aestivation type, several si®cation of Fritsch (1999, 2001). The ITS phylog- other characters diagnosed the deep divergences of eny was ambiguous as to the sectional the Styrax topology, whereas clades diagnosed by a classi®cation, although a combined analysis recov- reduced number of ovules per gynoecium were ered a topology consistent with it. A family-wide highly nested. In the recircumscribed sectional and phylogenetic analysis based on DNA sequences of series classi®cation, the clade corresponding to the the chloroplast genes rbcL and trnL-F in combi- Volume 90, Number 4 Huang et al. 493 2003 Revision of Styrax Series Cyrta nation with ITS sequences and morphology (Fritsch where (Gonsoulin, 1974; Fritsch, 1997; Fritsch, in et al., 2001) provided some support for section Sty- prep.), but are included in the key to species and rax, but support for section Valvatae was ambigu- various discussion sections to provide complete ous. The placement of Huodendron Rehder as sister coverage and facilitate identi®cation of cultivated to Styrax with strong support rendered the original material. state for corolla aestivation in the genus ambiguous because both genera are polymorphic for this char- GEOGRAPHIC DISTRIBUTION AND ENDEMISM acter. The monophyly of the subvalvate members of series Cyrta as predicted from morphology was not The 30 or so species of Styrax series Cyrta occur supported by the ITS results (Fritsch, 2001) be- in temperate lowland to tropical montane forests of cause several major clades contained both subval- eastern and southeastern Asia and North America vate and imbricate species. For example, S. japon- with 80±300 cm mean annual
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