HAN-QI YANG 1,2, HONG WANG 1,3 and DE-ZHU LI 1 *
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1 Botanical Journal of the Linnean Society, 2008, 156, With 36 figures Comparative morphology of the foliage leaf epidermis, with emphasis on papillae characters, in key taxa of woody bamboos of the Asian tropics (Poaceae: Bambusoideae) HAN-QI YANG 1,2, HONG WANG 1,3 and DE-ZHU LI 1 * 1 Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Heilongtan, Kunming, Yunnan , China 2 Department of Resources and Environment, Research Institute of Resource Insects of the Chinese Academy of Forestry, Bailongsi, Kunming, Yunnan , China 3 School of Life Science of Nanjing University, Nanjing , China Received December 2005; accepted for publication August 2007 The foliage leaf epidermis of 35 species representing 12 key genera of woody bamboos of the Asian tropics was investigated using light and scanning electron microscopy. The results indicated that papillae forms and distributional patterns around the stomatal apparatus of the abaxial foliage leaf epidermis were usually constant and were of great taxonomic significance at the specific and generic levels. However, papillae characters were not suitable for dividing subtribes within woody bamboos of the Asian tropics. On the basis of papillae characters, Schizostachyum s.s. and Cephalostachyum were confirmed, but their delimitations should be modified. The transfer of Leptocanna chinensis and Schizostachyum sanguineum into Cephalostachyum was supported, and Cephalostachyum virgatum and C. pergracile were confirmed to be members of Schizostachyum s.s. The subtribe Racemobambosinae did not obtain support and Racemobambos appeared to be better placed in subtribe Bambusinae. Neomicrocalamus was supported as a close relative and better treated as a synonym of Racemobambos. Gigantochloa was closely related to Dendrocalamus The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 156, ADDITIONAL KEYWORDS: generic delimitation scanning electron microscopy stomatal apparatus systematics. INTRODUCTION Molecular evidence indicates that the monophyly of woody bamboos, Bambuseae, consists of the temperate woody bamboo clade and the tropical woody bamboo clade; furthermore, the tropical woody bamboo clade can be divided into two subclades: the Old World tropical subclade and the New World tropical subclade (Clark, Zhang & Wendel, 1995; Zhang, 1996; Kelchner & Clark, 1997; Zhang & Clark, 2000). However, limited members of woody bamboos were *Corresponding author. dzl@mail.kib.ac.cn sampled in the previous molecular studies; therefore, the interrelationships within Bambuseae remain unclear. The Asian tropics possesses more than 300 native species of woody bamboo (Ohrnberger, 1999), and is a major distribution area of woody bamboos of the Old World tropical subclade (WBOWT) (Wu et al., 2003). Many attempts to establish the natural phylogeny of WBOWT, including woody bamboos of the Asian tropics (WBAT), have been made on the basis of morphological characters, in particular fruit and inflorescence characters. Munro (1868) divided WBAT into two sections (equivalent to subtribes in modern systems) on the basis of fruit characters, i.e. 411
2 412 H.-Q. YANG ET AL. Bambusae and Bacciferae. Bambusae consisted of four genera bearing caryopses: Bambusa Schreber, Gigantochloa Kurz ex Munro, Nastus Jussieu, and Oxytenanthera Munro. Bacciferae, which bore berrylike fruits, was subdivided into two subsections on the basis of inflorescence characters, i.e. Bambusoidea and Schizostachyoidea. Subsection Schizostachyoidea, which was characterized by having usually one floret per spikelet, included four genera: Cephalostachyum Munro, Melocanna Trinius, Pseudostachyum Munro, and Schizostachyum Nees. Subsection Bambusoidea comprised four genera usually bearing multiple florets per spikelet: Beesha Rheede, Dendrocalamus Nees, Dinochloa Buse, and Teinostachyum Munro. Bentham (1883) modified Munro s scheme and separated WBAT into three tribes: Eubambuseae (including Bambusa, Gigantochloa, Nastus, and Thyrsostachyum Gamble), Dendrocalameae (including Cephalostachyum, Dendrocalamus, Melocalamus Bentham, Pseudostachyum, and Teinostachyum), and Melocanneae (including Dinochloa, Melocanna, Ochlandra Thwaites, and Schizostachyum), which was followed by Gamble (1896). Holttum (1946) was the first author to describe the uniform structure of the ovaries in Cephalostachyum, Dendrochloa Parkinson, Neohouzeaua A. Camus, Pseudostachyum, Schizostachyum, and Teinostachyum, which included a long, hollow, stiff, and tapering ovary appendage (style) on top of the ovary, and suggested that they should be united into a broadly defined Schizostachyum s.l. Furthermore, Holttum (1956a) divided WBAT into two groups (equivalent to subtribes in modern systems) according to ovary type. The Schizostachyum group consisted of Melocanna, Schizostachyum s.l., and Ochlandra, and the Bambusa Dendrocalamus group included Bambusa, Dendrocalamus, Dinochloa, Gigantochloa, Melocalamus, and Thyrsostachyum. In the latter group, the top of the ovary was often attenuated to a slender, long or short and solid style usually covered with hairs. Since then, the ovary appendage has been regarded as an important character in dividing major clades within WBAT (for example, Clayton & Renvoize, 1986; Soderstrom & Ellis, 1987; Dransfield & Widjaja, 1995; Li, 1997). However, in the systems of Tzvelev (1989) and Keng & Wang (1996), which emphasized the significance of spikelets and fruits, Bambusa was placed in the tribe (= subtribe in other woody bamboo systems) Bambuseae, whereas Gigantochloa and Dendrocalamus were placed in the tribe Dendrocalameae. Meanwhile, Keng & Wang (1996) transferred Thyrsostachyum, Melocalamus, and Dinochloa to the tribe Melocanneae in Flora Reipublicae Popularis Sinicae. Within the genera described later in the subtribe Bambusinae, Neomicrocalamus Keng f. (Keng, 1983) was recognized synonymously with Racemobambos, which was established by Holttum (1956b). According to unique inflorescence features, Stapleton (1994a) established a new subtribe Racemobambosinae to accommodate Racemobambos. However, Clayton & Renvoize (1986), Tzvelev (1989), and Keng & Wang (1996) placed Racemobambos in Bambusinae. With regard to generic circumscriptions, Schizostachyum and its allies are complicated in WBAT. There are three different opinions. In the first, Holttum (1946, 1956a), followed by Clayton & Renvoize (1986), proposed to unite Schizostachyum, Cephalostachyum, Teinostachyum, Pseudostachyum, Neohouzeaua, and Dendrochloa in Schizostachyum s.l. This opinion emphasized the significance of ovary structure in the generic delimitation within Schizostachyum and its allies, and considered that the characters of florets and spikelets were not sufficient to support generic separation. In the second, totally opposite opinion, based on Munro (1868), several segregate genera, including Schizostachyum s.s., Teinostachyum, Neohouzeaua, Dendrochloa, Cephalostachyum, and Pseudostachyum, were proposed. This treatment was supported by Keng (1982), Soderstrom & Ellis (1987), Tzvelev (1989), Stapleton (1994b), Dransfield & Widjaja (1995), and Ohrnberger (1999). Third, Xia (1993) combined Teinostachyum, Neohouzeaua, Dendrochloa, and Leptocanna Chia and Fung with Schizostachyum. However, he treated Cephalostachyum, which had a dense capitulum and two stigmas, and Pseudostachyum, which had a long-necked rhizome and two stigmas, as independent genera. This treatment was followed by Keng & Wang (1996) and Li (1997), but the latter author separated Leptocanna. Leptocanna was published by Chia & Fung (1981) and was endemic to south-western China. It was distinguished from Schizostachyum s.s. by two glumes, three lodicules, and glabrous culms. As discussed above, previous studies of WBAT (for example, Munro, 1868; Bentham, 1883; Gamble, 1896; Tzvelev, 1989; Stapleton, 1994a; Dransfield & Widjaja, 1995; Keng & Wang, 1996; Ohrnberger, 1999), mainly based on inflorescence and fruit characters, are confusing and controversial. As pointed out by Clayton & Renvoize (1986), many woody bamboos flower periodically with intervals of years, and the spikelets of many bamboos are poorly known. As a result, many classifications of the subtribes or tribes of woody bamboos are based on insecure foundations. We have therefore initiated a survey of the key genera (Table 1) of WBAT, which are also core taxa of WBOWT, using morphological characters of the foliage leaf epidermis, in order to obtain some preliminary and reasonable solutions for the generic delimitation and phylogeny of the examined
3 TROPICAL ASIAN BAMBOO MORPHOLOGY 413 Table 1. Accessions that were examined morphologically Species No. of voucher Source Melocanna baccifera Kurz YHQ053 China: Guangdong Pseudostachyum polymorphum Munro YHQ016 China: Yunnan Leptocanna chinensis (Rendle) L. C. Chia and H. L. Fung YHQ042 China: Yunnan Cephalostachyum mannii (Gamble) Stapleton and D. Z. Li YHQ008 China: Yunnan Cephalostachyum scandens Bor YHQ011 China: Yunnan Cephalostachyum fuchsianum Gamble YHQ009 China: Yunnan Cephalostachyum pallidum Munro YHQ018 China: Yunnan Cephalostachyum pergracile Munro YHQ023 China: Yunnan Cephalostachyum virgatum Kurz YHQ014 China: Yunnan Schizostachyum blumei Munro KMW Malaysia Schizostachyum sanguineum W. P. Zhang Lu164 China: Yunnan Schizostachyum funghomii McClure YHQ028 China: Yunnan Schizostachyum pseudolima McClure YHQ041 China: Yunnan Schizostachyum hainanense Merr. ex McClure YHQ058 China: Hainan Schizostachyum jaculans Holttum YHQ059 China: Hainan Schizostachyum dumetorum Munro YHQ050 China: Guangdong Schizostachyum xinwuense T. H. Wen and J. Y. Chin YHQ047 China: Jiangxi Schizostachyum gracile (Munro) Holttum KMW Malaysia Schizostachyum zollingeri Steud. KMW Malaysia Melocalamus compactiflorus var. fimbriatus (Hsueh and C. M. Hui) YHQ017 China: Yunnan D. Z. Li and Z. H. Guo Melocalamus arrectus T. P. Yi YHQ015 China: Yunnan Melocalamus scandens Hsueh and C. M. Hui YHQ039 China: Yunnan Thyrsostachys oliveri Gamble YHQ027 China: Yunnan Thyrsostachys siamensis Gamble YHQ024 China: Yunnan Bambusa chungii McClure YHQ031 China: Yunnan Bambusa surrecta (Q. H. Dai) Q. H. Dai YHQ035 China: Yunnan Bambusa multiplex (Lour.) Raeusch. ex Schult. et Schult. f. YHQ013 China: Yunnan Dendrocalamus latiflorus Munro YHQ025 China: Yunnan Dendrocalamus strictus Nees YHQ052 China: Guangdong Dendrocalamus giganteus Munro YHQ012 China: Yunnan Gigantochloa verticillata Munro YHQ029 China: Yunnan Gigantochloa albociliata (Munro) Kurz DZL2004 Vietnam Racemobambos prainii (Gamble) Keng f. and T. H. Wen HYM202 China: Tibet Racemobambos yunnanensis T. H. Wen YHQ038 China: Yunnan Neomicrocalamus microphyllus Hsueh and T. P. Yi YHQ010 China: Yunnan Collectors are as follows: DZL, De-Zhu Li; HYM, Hai-Ying Ma; KMW, Khoon Meng Wong; Lu, Jin-Mei Lu; YHQ, Han-Qi Yang. Except for those in Malaysia, all voucher specimens were deposited at the herbarium of the Kunming Institute of Botany, Chinese Academy of Sciences (KUN). taxa, as part of a morphological and molecular study of Schizhostachyum and its allies. MATERIAL AND METHODS Thirty-five species from 12 genera, which covered the representative genera of WBAT, were sampled (Table 1). The materials of Schizostachyum blumei, S. zollingeri, and S. gracile were obtained from Professor Khoon Meng Wong (Malaysia). For practical purposes, we followed the classification scheme of Bambuseae in Flora Reipublicae Popularis Sinicae (Keng & Wang, 1996) with a few exceptions: Leptocanna chinensis, Racemobambos prainii, R. yunnanensis, Melocalamus compactiflorus var. fimbriatus, M. scandens, Cephalostachyum mannii, and C. scandens are based on the treatments of Flora Yunnanica (Li et al., 2003). The fresh foliage leaf materials for light microscopy (LM) and scanning electron microscopy (SEM) were fixed and preserved in formalin acetic alcohol (FAA). The examined sections described in this study were taken from the central part, about half-way between the apex and the base of the mature leaf lamina. The
4 414 H.-Q. YANG ET AL. materials for LM were boiled in water for min, and were then scraped according to the procedure described by Metcalfe (1960). To check the constancy of the epidermal structure, at least five slides were prepared from one to five foliage leaves for each species. Materials for SEM were submerged in xylene for at least 4 h in order to remove the waxy covering from the leaf epidermis, and were then attached directly to stubs without any treatment. After gold sputtering, the specimens were examined and photographed. The terminology of epidermis appendages follows Metcalfe (1960) and Chen SL, Jin & Wu (1993). RESULTS Under SEM, epidermal appendages, such as papillae, prickle-hairs, and bicellular microhairs, can be clearly observed. By contrast, the forms of short cells, long cells, and silica bodies are more conspicuous when examined with LM. Similar to the results of previous studies (for example, Metcalfe, 1960; Clark & Londono, 1991; Chen SL et al., 1993; Chen XY et al., 1993; Wang, Xia & Lin, 2002), the stomatal apparatus is obscured by overarching papillae in major examined species. As a result, the structures of the stomatal apparatus, such as guard cells and subsidiary cells, usually cannot be observed clearly. Therefore, we concentrate on a discussion of the papillae characters around the stomatal apparatus in this article. ADAXIAL FOLIAGE LEAF EPIDERMIS Long cells have thin and sinuous walls. Short cells are solitary or paired, and abundant. There is usually a row of dense or sparse papillae on the long cells and short cells of the examined species of Cephalostachyum and Schizostachyum s.s. Silica bodies are usually tall and narrow, rarely saddle-shaped. Bulliform cells are irregular polygonal (fan-shaped) or quadrilateral, with the length equal to or slightly longer than the width; there are usually two to five rows of bulliform cells between the veins. Bicellular microhairs are frequently observed, with the distal cell usually longer than the basal cell. Macrohairs and prickle-hairs are rarely seen. The stomatal apparatus is not, or rarely, seen. ABAXIAL FOLIAGE LEAF EPIDERMIS Long cells have thin and sinuous walls with the length conspicuously longer than the width. Short cells are solitary or paired, and abundant. Silica bodies are tall and narrow or saddle-shaped. Two to five rows of the stomatal apparatus usually occur between the veins. Bicellular microhairs, macrohairs, and prickle-hairs are commonly seen; in particular, hook-hairs are frequently seen. There are obvious variations in papillae forms and distributional patterns around the stomatal apparatus amongst the examined genera (Table 2), indicating their significant taxonomic value. Melocanna baccifera (Fig. 1) bears four rod-like papillae overarching each individual stomatal apparatus. Pseudostachyum polymorphum (Fig. 2) bears granular papillae surrounding each individual stomatal apparatus. Leptocanna chinensis (Fig. 3) bears four triangular papillae overarching each individual stomatal apparatus, and these four triangular papillae are again surrounded by eight to ten small granular papillae. In Cephalostachyum, the examined species can be divided into two groups. First, similar to L. chinensis, C. mannii (Fig. 4), C. scandens (Fig. 5), C. fuchsianum (Fig. 6), and C. pallidum (Fig. 7) bear four triangular or granular papillae overarching each individual stomatal apparatus, and these four triangular or granular papillae are again surrounded by 8 12 small granular papillae. Second, C. pergracile (Fig. 8) and C. virgatum (Fig. 9) bear four triangular papillae overarching each individual stomatal apparatus without surrounding small papillae. In Schizostachyum, S. sanguineum (Fig. 11) has almost identical papillae distributional patterns to L. chinensis. The remaining species of the examined Schizostachyum (Figs 10, 12 19), similar to C. pergracile and C. virgatum, usually bear four triangular papillae overarching each individual stomatal apparatus. These papillae overarching the stomatal apparatus are branched in S. jaculans (Fig. 15), S. dumetorum (Fig. 16), and S. gracile (Fig. 18). Each individual stomatal apparatus of M. compactiflorus var. fimbriatus (Fig. 20) and M. arrectus (Fig. 21) is surrounded by small granular papillae, and by six to ten small granular or rod-like papillae in M. scandens (Fig. 22). In Thyrsostachys, each individual stomatal apparatus is usually surrounded by four (in Th. oliveri; Fig. 23) or eight (in Th. siamensis; Fig. 24) granular papillae. In Bambusa, all examined species (Figs 25 27) bear four rod-like papillae overarching each individual stomatal apparatus. By contrast, all examined species of Dendrocalamus (Figs 28 30) and Gigantochloa (Figs 31, 32) have eight rod-like or granular papillae overarching each individual stomatal apparatus. Both R. prainii (Fig. 33) and Neomicrocalamus microphyllus (Fig. 35), similar to the examined species of Bambusa, bear four rod-like papillae overarching each individual stomatal apparatus. However, each individual stomatal apparatus of R. yunnanensis (Figs 34, 36) is surrounded by eight to ten granular or rod-like papillae.
5 TROPICAL ASIAN BAMBOO MORPHOLOGY 415 Table 2. Papillae characters of abaxial foliage leaf epidermis (scanning electron microscopy) Genus Species Papillae forms and distributional patterns around the stomatal apparatus Figure Melocanna M. baccifera 4, rod-like, overarching Fig. 1 Pseudostachyum P. polymorphum 10 16, granular, around stomatal apparatus Fig. 2 Leptocanna L. chinensis 4, triangular and overarching, and surrounded Fig. 3 by 8 10 small granular papillae Cephalostachyum C. mannii 4, granular and overarching, and surrounded Fig. 4 by small granular papillae C. scandens 4, triangular and overarching, and surrounded Fig. 5 by 8 10 small granular papillae C. fuchsianum 4, triangular and overarching, and surrounded Fig. 6 by 8 12 small granular papillae C. pallidum 4, triangular and overarching, and surrounded Fig. 7 by 8 10 small granular papillae C. pergracile 4, triangular and overarching Fig. 8 C. virgatum 4, triangular and overarching Fig. 9 Schizostachyum S. blumei 4, triangular and overarching Fig. 10 S. sanguineum 4, triangular and overarching, and surrounded Fig. 11 by 8 12 small granular papillae S. funghomii 4, triangular and overarching Fig. 12 S. pseudolima 4, triangular and overarching Fig. 13 S. hainanense 4, triangular and overarching Fig. 14 S. jaculans 4, triangular, branched, and overarching Fig. 15 S. dumetorum 4, triangular, branched, and overarching Fig. 16 S. xinwuense 4, triangular and overarching Fig. 17 S. gracile 4, triangular, branched, and overarching Fig. 18 S. zollingeri 4, triangular and overarching Fig. 19 Melocalamus M. compactiflorus var. fimbriatus 14 16, granular, around stomatal apparatus Fig. 20 M. arrectus 14 16, granular, around stomatal apparatus Fig. 21 M. scandens 6 10, granular or rod-like, around stomatal Fig. 22 apparatus Thyrsostachys Th. oliveri 4, granular, around stomatal apparatus Fig. 23 Th. siamensis 8, granular, around stomatal apparatus Fig. 24 Bambusa B. chungii 4, rod-like, overarching Fig. 25 B. surrecta 4, rod-like, overarching Fig. 26 B. multiplex 4, rod-like, overarching Fig. 27 Dendrocalamus D. latiflorus 8, rod-like or granular, overarching Fig. 28 D. strictus 8, rod-like or granular, overarching Fig. 29 D. giganteus 8, rod-like or granular, overarching Fig. 30 Gigantochloa G. verticillata 8, rod-like or granular, overarching Fig. 31 G. albociliata 8, rod-like or granular, overarching Fig. 32 Racemobambos R. prainii 4, rod-like, overarching Fig. 33 R. yunnanensis 8 10, granular or rod-like, around stomatal Figs 34, 36 apparatus Neomicrocalamus N. microphyllus 4, rod-like, overarching Fig. 35 DISCUSSION TAXONOMIC VALUE OF PAPILLAE CHARACTERS IN WBAT The leaf epidermal characters of woody bamboos in general, and the papillae forms and distributional patterns on the abaxial foliage leaf epidermis in particular, have been proven to be of taxonomic value at the specific, generic, and subtribal levels (for example, Metcalfe, 1960; Soderstrom & Ellis, 1987; Clark, 1990; Clark & Londono, 1991; Chen SL et al., 1993, Chen XY et al., 1993; Lu, 1996; Wang et al., 2002). In the current study, epidermal features were again constant within species, and therefore presented good characters for taxonomy at the generic level. On the basis of papillae characters, our results support the
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7 TROPICAL ASIAN BAMBOO MORPHOLOGY 417 Figures Micromorphology of papillae on abaxial leaf epidermis (scanning electron microscopy). Fig. 1. Melocanna baccifera. Fig. 2. Pseudostachyum polymorphum. Fig. 3. Leptocanna chinensis. Fig. 4. Cephalostachyum mannii. Fig. 5. Cephalostachyum scandens. Fig. 6. Cephalostachyum fuchsianum. Fig. 7. Cephalostachyum pallidum. Fig. 8. Cephalostachyum pergracile. Fig. 9. Cephalostachyum virgatum. Fig. 10. Schizostachyum blumei. Fig. 11. Schizostachyum sanguineum. Fig. 12. Schizostachyum funghomii. Scale bars, 10 mm. White arrows indicate the opening of the stomatal apparatus. small genus perspective in generic circumscriptions within Melocanninae (e.g. Soderstrom & Ellis, 1987; Xia, 1993; Keng & Wang, 1996; Li, 1997; Ohrnberger, 1999; Li et al., 2003). Cephalostachyum (better including Leptocanna), Melocanna, Pseudostachyum, and Schizostachyum s.s. were confirmed on the basis of papillae forms and distributional patterns around the stomatal apparatus, but the circumscriptions of Cephalostachyum and Schizostachyum s.s. should be modified. Within the woody bamboos (Bambuseae), foliage leaf epidermal micromorphology is useful in dividing subtribes (Soderstrom & Ellis, 1987). In this study, although the form and distributional patterns of papillae showed great taxonomic value at the generic level, our results suggested that the papillae characters were not suitable for the division of subtribes within WBAT. The traditional delimitations of Bambusinae and Melocanninae (for example, Holttum, 1956a; Clayton & Renvoize, 1986; Soderstrom & Ellis, 1987; Dransfield & Widjaja, 1995; Li, 1997; Ohrnberger, 1999) were not supported by papillae characters. Melocanna baccifera, R. prainii, and Neomicrocalamus microphyllus showed almost identical papillae forms and distributional patterns to the examined species of Bambusa, and the papillae characters of Pseudostachyum were similar to those of Melocalamus. The subtribe Racemobambosinae (Stapleton, 1994a) appeared to be better placed in Bambusinae. Indeed, the results based on papillae form and distributional pattern in the current study were congruent with our recent molecular phylogenetic study of WBAT, using the markers of the nuclear granule-bound starch synthase I (GBSSI) gene and chloroplast trnl-f sequences (Yang, Peng & Li, 2007). In addition, with increasing habitat elevation, the distributional patterns of the papillae above and around the stomatal apparatus on the abaxial foliage leaf epidermis became more and more complicated, and the stomatal opening was more and more tightly covered and protected. The genera of lower habitat elevations, such as Schizostachyum and Bambusa, bore only four triangular or rod-like papillae overarching the stomatal apparatus without other appendages above the stomatal apparatus. However, within the species and genera at higher habitat elevations, such as Leptocanna and the majority of the examined species of Cephalostachyum, the opening of the stomatal apparatus was almost completely covered by papillae and cuticula, and these papillae were usually surrounded by some small papillae. This may be an adaptation of the stomatal apparatus to reduce water loss and to increase water use efficiency (Serna, 2001). LEAF EPIDERMIS EVIDENCE FOR CEPHALOSTACHYUM The papillae characters on the abaxial epidermis within L. chinensis, S. sanguineum, and all examined species of Cephalostachyum, excluding C. virgatum and C. pergracile, were nearly uniform, namely, these species usually bore four triangular (granular in C. mannii) papillae overarching each individual stomatal apparatus, and these papillae were again surrounded by 8 12 small granular papillae. Our results supported the treatments of Stapleton, Li & Xue (1997) that combined Arundinaria mannii into Cephalostachyum as C. mannii on the basis of morphological characters. Meanwhile, our results also confirmed that C. scandens should be a member of Cephalostachyum. Although C. scandens was morphologically similar to Schizostachyum s.s., different papillae characters, as well as the presence of a capitulum (Li & Guo, 2000; Li et al., 2003), indicated that this species did not belong to Schizostachyum s.s. Gamble (1896) divided Cephalostachyum into two sections according to inflorescences. Section I included the type species, C. capitatum, and species, such as C. fuchsianum and C. pallidum, which were characterized by spikelets in single terminal globose heads. Section II, which was described as having spikelets in heads in interrupted paniculate spikes, included C. pergracile and C. virgatum. In fact, the inflorescences of C. pergracile and C. virgatum are very similar to those of Schizostachyum s.s., such as S. zollingeri, S. brachycladum, S. jaculans, and S. hainanense, whose inflorescences consist of dense tufts of pseudospikelets at the nodes of the flowering branches (Dransfield & Widjaja, 1995; Keng & Wang, 1996). In addition to the discrepancy in the inflorescences, C. virgatum and C. pergracile are erect bamboos, bear three stigmas, and occur at lower
8 418 H.-Q. YANG ET AL.
9 TROPICAL ASIAN BAMBOO MORPHOLOGY 419 Figures Micromorphology of papillae on abaxial leaf epidermis (scanning electron microscopy). Fig. 13. Schizostachyum pseudolima. Fig. 14. Schizostachyum hainanense. Fig. 15. Schizostachyum jaculans. Fig. 16. Schizostachyum dumetorum. Fig. 17. Schizostachyum xinwuense. Fig. 18. Schizostachyum gracile. Fig. 19. Schizostachyum zollingeri. Fig. 20. Melocalamus compactiflorus var. fimbriatus. Fig. 21. Melocalamus arrectus. Fig. 22. Melocalamus scandens. Fig. 23. Thyrsostachys oliveri. Fig. 24. Thyrsostachys siamensis. Scale bars, 10 mm. White arrows indicate the opening of the stomatal apparatus. elevations (usually below 1200 m) (Keng & Wang, 1996), which distinguishes them from the other examined species of Cephalostachyum. It seems more appropriate to separate Gamble s section II from Cephalostachyum on the basis of the papillae and morphological characters. Leptocanna chinensis has generally been regarded as a member of Schizostachyum s.s. (for example, Clayton & Renvoize, 1986; Xia, 1993; Keng & Wang, 1996; Ohrnberger, 1999) or a monotypic genus (for example, Chia & Fung, 1981; Soderstrom & Ellis, 1987; Tzvelev, 1989; Li, 1997; Li et al., 2003). In this study, L. chinensis was placed into Cephalostachyum on the basis of papillae characters. In the floret structure, both L. chinensis and typical Cephalostachyum have two glumes and three lodicules. Moreover, L. chinensis is apically pendulous, and occurs at higher elevations ( m) with cold temperate habitats, similar to the majority of the examined Cephalostachyum. Schizostachyum sanguineum, described by Zhang (1989) on the basis of specimens without inflorescences and fruits, is an apically climbing bamboo and occurs in habitats at an elevation of 1600 m. The similar habit implies that S. sanguineum belongs to Cephalostachyum (Yang & Li, 2007). Therefore, newly circumscribed Cephalostachyum may be limited to members that: (1) have a shrubby or subarborescent habit usually apically pendulous or climbing; (2) occur in habitats at an elevation of c m; (3) bear a terminal inflorescence (capitulum or panicle); (4) have spikelets with two or three glumes; (5) have florets with two stigmas and two or three lodicules; and (6) usually bear four triangular or granular papillae overarching each individual stomatal apparatus, with these papillae surrounded by 8 12 small granular papillae. Soderstrom & Ellis (1987) did not regard the species of Cephalostachyum of Malagasy and of the Himalaya to be congeneric, because the species of the former region are vines and their branching habit is quite different from that of the species from the Himalaya. Our results partly support their inferences. All of the examined species in our newly delimited Cephalostachyum are usually pendulous or climbing at the top. However, to clarify the delimitation and systematic position of Cephalostachyum, further research based on comprehensive evidence is required. LEAF EPIDERMIS EVIDENCE FOR SCHIZOSTACHYUM S.S. In the current study, C. pergracile, C. virgatum, and the examined species of Schizostachyum, except S. sanguineum, show almost the same papillae characters, i.e. each individual stomatal apparatus is overarched by four branched or unbranched triangular papillae. As discussed above, C. virgatum and C. pergracile share many common morphological characters with Schizostachyum s.s., and it seems more appropriate for them to be placed in Schizostachyum s.s. Meanwhile, S. sanguineum should be transferred into Cephalostachyum based on the similar habit and papillae characters. Then, Schizostachyum may be limited to species with the following similar morphological characters: (1) distributed in habitats with an elevation usually below c m; (2) bear a panicle consisting of densely or slightly glomerate spikelets on the nodes of the flowering branches; (3) have the glumes usually absent; (4) bear florets with three stigmas and usually without lodicules; and (5) usually bear four triangular papillae overarching each individual stomatal apparatus. LEAF EPIDERMIS EVIDENCE FOR MELOCANNA AND PSEUDOSTACHYUM Although the papillae characters of Melocanna and Pseudostachyum, two monotypic genera (some authors believe that these two genera both include two species; e.g. Ohrnberger, 1999), were not unique in the results of the current study, if considered within subtribe Melocanninae, the papillae characters undoubtedly demonstrate their autapomorphy. Morphologically, the florets of Melocanna have two lodicules, and the fruit is pear-like, long beaked at the apex, without endosperm, and usually viviparous. By contrast, in Pseudostachyum, the florets have three to five lodicules, and the fruit is compressed globose, nut-like, with a crustaceous pericarp which is easily separated with the seeds. All of these characters imply that Melocanna and Pseudostachyum represent two good genera. RELATIONSHIP BETWEEN BAMBUSA AND DENDROCALAMUS These two vegetatively similar genera can be easily distinguished by their papillae characters. In the
10 420 H.-Q. YANG ET AL.
11 TROPICAL ASIAN BAMBOO MORPHOLOGY 421 Figures Micromorphology of papillae on abaxial leaf epidermis (scanning electron microscopy). Fig. 25. Bambusa chungii. Fig. 26. Bambusa surrecta. Fig. 27. Bambusa multiplex. Fig. 28. Dendrocalamus latiflorus. Fig. 29. Dendrocalamus strictus. Fig. 30. Dendrocalamus giganteus. Fig. 31. Gigantochloa verticillata. Fig. 32. Gigantochloa albociliata. Fig. 33. Racemobambos prainii. Fig. 34. Racemobambos yunnanensis. Fig. 35. Neomicrocalamus microphyllus. Fig. 36. Racemobambos yunnanensis. Scale bars, 10 mm. examined species of Bambusa, each individual stomatal apparatus is overarched by four rod-like papillae, whereas, in Dendrocalamus, it is overarched by eight rod-like or granular papillae. The main differences in the papillae characters between these two genera lie in the quantity of papillae overarching the stomatal apparatus, implying that there is a close relationship between Bambusa and Dendrocalamus. Holttum (1946, 1956a) considered Bambusa to be closely related to Dendrocalamus on the basis of the similar structures of the fruits and ovary appendages. He distinguished Dendrocalamus and Bambusa by the development of rachilla in the pseudospikelets. In Bambusa, the rachilla is elongated and jointed, with several internodes usually 2 mm or longer, and the lemmas of the fertile florets are all of about the same length. However, in Dendrocalamus, the rachilla is very short and not jointed; moreover, the lower lemmas are shorter than the upper. This criterion was accepted by McClure (1966), Chia & Fung (1980), Keng (1982), Clayton & Renvoize (1986), Li & Hsueh (1988), Li (1994), Soderstrom & Ellis (1987), and Stapleton (1994b). RELATIONSHIP BETWEEN GIGANTOCHLOA AND DENDROCALAMUS Gigantochloa is similar to Dendrocalamus in vegetative appearance. They show an almost uniform inflorescence structure, namely, the internodes of the rachilla are usually very short and not jointed below the lemmas, and the florets are crowded closely on the rachilla (Holttum, 1946, 1956a). Taxonomically, Gigantochloa was separated from Dendrocalamus mainly because the florets of Gigantochloa showed a well-developed stamen tube (Holttum, 1946). In this study, the papillae characters of Gigantochloa and Dendrocalamus were almost identical, i.e. each individual stomatal apparatus was overarched by eight rod-like or granular papillae. This result indicates that Gigantochloa is closely related to Dendrocalamus, and implies that the treatment of Soderstrom & Ellis (1987), which united Gigantochloa into Dendrocalamus, is reasonable. RELATIONSHIP BETWEEN RACEMOBAMBOS AND NEOMICROCALAMUS The papillae form and distributional pattern of these two vegetatively similar species, Neomicrocalamus microphyllus and R. prainii, are uniform. Their papillae characters seem to support the opinions of Wen (1986) and Clayton & Renvoize (1986), who regarded Neomicrocalamus to be synonymous with Racemobambos, and the treatment of Li et al. (2003), who recognized Neomicrocalamus microphyllus and R. prainii as conspecific. The arguments about Neomicrocalamus and Racemobambos have focused on their inflorescences. Dransfield (1983) and Clayton & Renvoize (1986) regarded the inflorescences of Racemobambos as determinate. However, in Racemobambos, the buds occasionally occur under the bracts, although these buds have never been observed to develop; therefore, Chao & Renvoize (1988) and Li et al. (2003) considered the inflorescences of Racemobambos to be indeterminate, similar to Keng s (1983) Neomicrocalamus. Our results seem to support the latter opinion. In addition, R. yunnanensis, a climbing bamboo described by Wen (1986) on the basis of a specimen without inflorescences and fruits, does not seem to be congeneric with R. prainii, but appears to be closely related to Melocalamus, on the basis of similar papillae characters. However, to clarify the taxonomic position of R. yunnanensis, more studies based on broader sampling and evidence are required. ACKNOWLEDGEMENTS We are grateful to Professor Khoon Meng Wong (Institute of Biological Sciences, University of Malaya), Drs Nian-He Xia and Yun-Fei Deng (South China Botanical Garden, Chinese Academy of Sciences), Mr Bin Wen and Dr Ling Zhang (Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences), and Dr Chao-Mao Hui (South-west Forestry College, Kunming) for help in collecting experimental material. We also wish to express our thanks to Ms. Chun-Fang Li and Hong-Ping Ma for assistance. This work was funded by the Yunnan Provincial Government through an Award for Prominent Contributions in Science and Technology to Professor Wu Zheng-Yi in 2001 (grant no. KIB-WU ), the projects of the Ministry of Science and Technology of China (grant nos. 2005DKA21006 and 2006BAD19B03), and the National Natural Science Foundation of China (grant no to Z. H. Guo and grant no to Hong Wang).
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