Floristics and Plant Biogeography in China
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1 Floristics and Plant Biogeography in China De-Zhu Li* (Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, the Chinese Academy of Sciences, Kunming , China; Plant Germplasm and Genomics Center, the Germplasm Bank of Wild Species, Kunming , China) (This invited review is dedicated to Prof. C. Y. Wu**, winner of the 2007 National Supreme Science and Technology Award of China, on the occasion of his 92nd birthday and 71 st anniversary of botanical research) *Author for correspondence. Tel: ; **Wu Cheng Yih in Wide-Giles transliteration, as Wu Zhengyi or Wu Zheng Yi in Hanyu Pinyin transliteration. Supported by the National Basic Research Program of China (973 Program 2007CB411601) and the Yunnan Provincial Government through an Award for Prominent Contributions in Science and Technology to Prof. Wu Zheng-Yi in Abstract In 1998, a revolutionary system of angiosperm classification, the APG system was published. Meanwhile, another new system of classification of angiosperms, the eight-class system was proposed by C. Y. Wu and colleagues based on the long time work on the flora of China. The Flora Reipublicae Popularis Sinicae (FRPS, thereafter) project was initiated in 1959 and completed by It is the largest Flora so far completed in the world, including some 31,228 species of vascular plants, or one-eighth of the global plant diversity. The English-language and updated Flora of China (FOC) is an international joint effort initiated in 1988 and accelerated in Up to now, fifteen out of the 25 volumes of the FOC have been published. Based on the floristic data, the composition, characteristics, floristic divisions and affinities of the flora of China have been studied by Wu and colleagues since In the past ten years, analyses of the available floristic data were very productive. The East Asiatic Floristic Kingdom was proposed in All 346 families of angiosperms in China according to the eight-class system of 1
2 classification were comprehensively discussed by using knowledge of current and historical distribution of seed plants in the world, together with some morphological and molecular data. A scheme of distribution patterns or areal-types of families and genera of seed plants in China was modified and elucidated, together with a proposed scheme of areal-types of the world. Molecular phylogenetic and biogeographic studies of angiosperms in China in the past ten years also witnessed a progressive development. Integration of morphological and molecular data and fossil evidence revealed some significant results. Eastern Asia, which used to be regarded as an important center of survival during the ice age, is likely an important center of diversification of angiosperms. Key words: floristics; phylogenetics; biogeography; Center of diversification; Eastern Asia The diversity and evolution of plants, the primary producers of global ecosystems have long puzzled plant biologists since the time of Darwin, when evolution became the centerpiece of biology. Although Linnaeus sexual system of plants has long been regarded as an artificial system, efforts to establish a natural system of classification of the angiosperms, or the flowering plants, only began achieving an ultimate consensus ten years ago. Following the joint paper of a large teamwork on the phylogenetics of seed plants based on analysis of chloroplast rbcl gene sequences of 499 plants (Chase et al. 1993), twenty-nine worldwide botanists initiated an Angiosperm Phylogeny Group (APG 1998) who proposed an entirely new system of angiosperms based on molecular data. This was a great breakthrough in the study of phylogenetics of plants. Five years later, in the explanation of their updated system (APG-II 2003), it was stated that the then widely used classifications, such as those of Cronquist (1981), Thorne (1992) and Takhtajan (1997) were based on selected similarities and differences in morphology rather than cladistic analysis of larger data sets including DNA sequences or other forms of systematic data. This revolutionary system of classification of angiosperms was published in December 1998 (the fourth issue of the Annals of the Missouri Botanical Garden). Wu and colleagues analyzed the distribution patterns of the Magnoliidae and pointed out the possibility and necessity of a polyphyletic-polychronic-polytopic system of classification of angiosperms (Wu et al. 1998a). Slightly earlier, based on the long time work on the flora of China, an eight-class system of classification of the angiosperms was proposed by Wu et al. (Wu et al. 1998b) in a less-widely 2
3 circulated journal, Acta Phytotaxonomica Sinica (the fifth issue of the journal, in October). In their paper, it is stressed that the current subdivision of the angiosperms into two major groups, the dicotyledons and the monocotyledons, whether at the rank of class or subclass, is greatly challenged by more and more evidence from comparative morphology, chemotaxonomy, paleobotany, cladistics and molecular systematics. Although the later was regarded as basically following that proposed by Takhtajan (1997) by APG-II, the revolutionary change of the major subgroups of the angiosperms in this eight-class system was, in fact, closer in consensus with the APG system than that of Takhtajan (1997) in which two classes, Magnoliopsida and Liliopsida (i.e., dicots and monocots) were still recognized. The differences between the APG system and the eight-class system are substantial. However, in methodology, the APG system is based primarily on cladistic analysis of molecular sequence data using computer-based programmes, while the eight-class system is derived from morphological and molecular data with special reference to data of modern geographical distributions, in a more or less selective way. Both systems follow the Linnean hierarchy, but the APG system emphasizes the rank order whereas the eight-class system prefers the more traditional rank class. Another subtle difference is that the authors of the APG systems are mainly molecular-and-morphological-based botanists while those of the eight class system are mainly old generation botanists. The first author is Prof. C. Y. Wu, who was then 82-year old and led the first-ever entire series of FRPS to completion in Because floristic data is very crucial to phytogeographical analyses and the study of systems of classification, as well as to biodiversity conservation and sustainable use of plant resources, much effort has been put into floristics since botany emerged in modern China. Floristics Early Floristic work The flora of China is the most diverse in the North Temperate zone and is one of the richest in the world. European botanists who conducted botanical explorations in China more than 200 years ago were amazed by the beauty and the diversity of Chinese plants. Although a few of the earlier western and Chinese botanists made individual effort to write some catalogs and incomplete flora of China, it was not until about the middle of the last century that Chinese 3
4 botanists began to make a collective effort to publish a national flora. The pioneer of such a flora is Dr. H. H. Hu, one of the founders of the modern botany in China, who received his PhD degree in the Harvard University in Hu s PhD dissertation was Synopsis of Chinese genera of phanerogams, with descriptions of representative species (Ma and Barringer 2005). After being elected as the President of Botanical Society of China in 1934, of which he was one of the founders, he made a proposal for the compilation of a national flora of China. Although this was not achieved at that time, taxonomic studies of Chinese plants were established by 1940s in the pteridophytes (R. C. Ching), gymnosperms (W. C. Cheng) and major families of angiosperms, such as the Aceraceae and Ericaceae (W. P. Fang), Annonaceae, Apocynaceae and Asclepiadaceae (Y. Tsiang), Araliaceae (H. L. Li and C. Ho), Begoniaceae and Rosaceae (T. T. Yu), Betulaceae, Proteaceae, Styracaceae, Theaceae and Ulmaceae (H. H. Hu), Campanulaceae (P. C. Tsoong), Chenopodiaceae and Polygonaceae (H. W. Kung & C. P. Tsien), Compositae (Y. Ling & C. C. Chang), Cruciferae (T. Y. Chou), Dioscoreaceae and Verbenaceae (C. Pei), Fagaceae, Gesneriaceae and Lauraceae (W. Y. Chun), Gramineae (Y. L. Keng), Juglandaceae and Myricaceae (K. C. Kuan), Orchidaceae and Liliaceae (F. T. Wang & C. Tang), Papaveraceae and Labiatae (C. Y. Wu), Primulaceae (F. H. Chen), Rubiaceae (F. C. How), Scrophulariaceae (H. L. Li & P. C. Tsoong) and Umbelliferae (R. H. Shan). During that time, R. C. Ching photographed some 20,000 Chinese (mostly type) specimens in the herbarium of Royal Botanic Gardens Kew and other major herbaria in Sweden and Austria. With the support of his mentor W. C. Wu, C. Y. Wu made about 30,000 cards recording original literature of Chinese plant names which were linked to specimen photos by R. C. Ching with special reference to Symbolae Sinicae (Handel-Mazzetti ). The Ching photos and the Wu cards became very precious reference for the initiation of a national-wide flora. In 1950, the newly organized Chinese Academy of Sciences (CAS, originally as Academia Sinica) convened a meeting on plant taxonomy and formally called on the need of compilation of a national flora of China. Subsequently, Claves Familiarum Generumque Plantarum Sinicarum was published in Acta Phytotaxonomica Sinica (vols. 2-4) in Simplified and illustrated floras for some major families were published, i.e., Illustrated Treatment of the Principal Plants of China, Leguminosae (Wang and Tang 1955), Illustrations of Important Chinese Plants, Pteridophytes (Fu 1957), and Flora Illustralis Plantarum Primarum Sinicarum- Gramineae (Keng 1959). Interestingly, these three published floras with the same Chinese title 4
5 were given totally different English or Latin ones. A brief of the Flora Reipublicae Popularis Sinicae project In 1959, Drs. S. S. Chien, H. H. Hu and other 24 botanists made a formal proposal and the CAS initiated the Flora Reipublicae Popularis Sinicae (FRPS, hereafter) project for a Chinese-language version of the flora of China. Drs. S. S. Chien (CAS Institute of Botany) and W. Y. Chun (CAS South China Institute of Botany) were appointed to the editors-in-chief, with R. C. Ching being the secretary-general of the editorial committee composed of twenty-five members, mostly first generation botanists of China. The first published volume of FRPS was volume 2 (Pteridophytes, part 1) (Ching 1959). The second published volume was volume 11 (Cyperaceae, part 1) (Tang and Wang 1961), and the third being volume 68 (Scrophulariaceae, part 2) (Tsoong 1963). However, because of the Cultural Revolution, there was nothing published for the FRPS during 1964 to CAS called a meeting on the compilation of a national Flora and a national Fauna in By that time, both editors-in-chief of the FRPS had passed away. R. Ling (CAS Institute of Botany) was designated as the editor-in-chief, C. Y. Wu, H. B. Cui, C. P. Tsien and H. Y. Hong as the associate editors-in-chief. Some middle-aged botanists were appointed to the second editorial committee. As a result, volume 36 (Rosaceae, part 1) (Yu 1974) was published. Accounts of three more families were subsequently published, i.e., Apocynaceae and Asclepiadaceae (Tsiang and Li 1977) and Labiatae (Wu and Li 1977a, b). After the Cultural Revolution, the compilation work on the Flora entered into a gold era. In 1977, T. T. Yu (CAS Institute of Botany) was appointed to the third editor-in-chief, and C. Y. Wu and H. B. Cui were the associate editors-in-chief. The editorial committee was enlarged to include some 40 members, representing 27 botanical research institutions or departments in universities. Three volumes were published in 1978, and ten volumes in Until 1986, some 41 books in 36 volumes were published with some 10,958 species treated. After the death of T. T. Yu in 1986, C. Y. Wu (CAS Kunming Institute of Botany) was appointed to the fourth editor-in-chief of the editorial committee, with H. B. Cui as the associate editor-in-chief, and other 21 members. By that time, some of the major families such as Compositae, Gramineae, Orchidaceae, Leguminosae, Ericaceae and Rubiaceae were still under compilation. Much effort was put into these and other difficult families. In 1996, the editorial committee was reorganized by including only 18 members 5
6 with 7 senior consultants. Even so, all members were at the age of 60 or above. The shortage of young and qualified taxonomists threatened the project. Some 44 books in 35 volumes remained unpublished. To ensure the completion of this project, four younger botanists were designated to members of the committee in Eventually, in September 2004, all 126 books of the 80 volumes of this magnum opus were published (Yang et al. 2005). This monumental work is very much the fruit of longtime teamwork, lasting for more than 45 years, involving 312 botanists in three generations and 164 artists who made some 9081 line illustrations. Statistics shows that some species of 344 genera in 302 families were included in the FRPS. After excluding 48 species of 10 genera of 2 families which were repeatedly treated, the number of vascular plants in the FRPS is species of 3434 genera in 300 families (Ma and Clemants 2006). Prof. C. Y. Wu played the most important role in and made critical contributions to the FRPS project. He was the founding member of the first editorial committee during , associate editor-in-chief during , and editor-in-chief during (Wu and Chen 2004). He witnessed all stages of the project and led major part of the project into completion. Under his editorship, 82 books of 54 volumes of the FRPS were published since 1987, treating some species of 2019 genera of 166 families. His knowledge of Chinese plant diversity is well received by the botanical circle of the world. The Flora of China project: an Update Because the FRPS was written in Chinese, and was not readily accessible to the people who can not read Chinese, an English-language Flora of China was needed. Furthermore, as the FRPS started in 1959, most authors were not able to write their accounts of species described prior to 1950s against their type specimens deposited in western herbaria. This to some extent made it difficult to accurately apply published names to specimens collected after 1950s. In 1979, a Chinese botanical delegation, the first of this kind since the Cultural Revolution, visited the United States. Members of the delegation, T. T. Yu and C. Y. Wu proposed that a project be started to revise the FRPS through an international collaborative project. During the 1987 International Botanical Congress in Berlin, with the approval of CAS, C. Y. Wu discussed with Peter H. Raven, Director of the Missouri Botanical Garden details of the collaboration and agreed in general an international project between the Chinese Academy of Sciences and the Missouri Botanical 6
7 Garden. This eventually became the Flora of China (FOC) project which officially commenced in the autumn of 1988, and Wu and Raven became the co-chairs of the joint editorial committee, who signed a formal agreement under a tree of Metasequoia glyptostroboides on 7 October 1988 in the Missouri Botanical Garden, USA. This project provides unique opportunities for collaboration among hundreds of Chinese and non-chinese botanists and is an important step for introducing the flora of China to the world. The FOC is designed to be published in 25 volumes of text, together with 25 volumes of accompanying illustrations. It follows the same sequences of families as in FRPS, which is a modified Englerian System that treated the monocots after the dicots. Volume 17 is the first text one to be published in the series and treats families Verbenaceae, Lamiaceae and Solanaceae (Wu and Raven 1994), followed by volumes 16 and 15 which were published in 1995 and 1996, respectively. The first accompanying illustration volume (Flora of China Illustrations, volume 17) was published in Twelve additional text volumes and 11 additional illustration volumes have been published since During the joint editorial committee meeting in August 2001 in Kunming, Prof. Y. Y. Chen, Vice President of the CAS, and Dr. Peter H. Raven, Director of the Missouri Botanical Garden, signed a new contract on the project for the next five years. After the Kunming meeting, Prof. D. Y. Hong was nominated to be the vice co-chair of the joint editorial committee which replaced the first one in 2002 to include some middle-aged botanists from China. Up to now, 15 out of the 25-volumed text books were published, treating 19,318 species of seed plants, among which 10,147 species or 52.53% were endemic to China. According to statistics from the latest meeting of the joint editorial committee in Hangzhou in April 2008, accounts of some 30,266 out of an estimate of 31,318 species (or 96.64%) of vascular plants were submitted to the editorial centers. It is planned that all 25 volumes will be published by Revisions were made in various families in the FOC. For example, the grass volumes in FRPS, volumes 9(1), 9(2), 9(3), 10(1) and 10(2) treated some 1,942 species of 247 genera, while the single FOC grass volume, volume 22 (Wu et al. 2006a) recognized 1,795 species of 226 genera with large number of species not recorded in FRPS. Because of the significant role of Chinese flora, the publication of FOC will greatly contribute to the botanical circle of the world (Wu 1989). The FOC will not only provide botanists around the world an English-language flora of China, but also an update of knowledge of plant 7
8 taxonomy and phytogeography in China. The Use of Floristic Data in Phylogenetics and Biogeography Phylogenetics is the study of evolutionary relationships among species and higher taxonomic ranks of organisms, and provides important information on patterns of inferred genetic similarity in time and space. Biogeography is the study of distribution of organisms in time and space. Source of floristic data includes published national and regional texts that summarize taxonomic relationships, provide discussion of taxa, and give brief geographical and ecological data pertinent to the taxa of the area covered (Morin et al. 1989). Phytogeographic Analyses The study of phytogeography in China can be traced back into 1913 when Diels published his paper on the plant distributions in West China (Wu et al. 2006b). C. Y. Wu and colleagues studied the composition, characteristics, floristic divisions and affinities of the flora of China, based on the then available floristic data (Wu 1965; Wu 1979; Wu and Wang 1983). Wu has developed an analytic approach in phytogeography that has been widely used in China and elsewhere (Qian 1998). In the past five years or so, C. Y. Wu and colleagues published a series of papers or books on the phytogeography of China (Wu and Wu 1998; Wu et al. 2003a; Wu et al. 2003b; Wu et al. 2005; Wu et al. 2006b). Based on the floristic data of FRPS, FOC and other available regional floras of China, Wu et al. (2003a) comprehensively discussed all 346 families of angiosperms in China according to the eight-class system of classification, by using current knowledge of modern and historical distribution of flowering plants in the world, together with some morphological and molecular data. Based on an analysis of distribution patterns of some 3000 genera of seed plants in China, Wu established a scheme of classification of distribution patterns or areal-types of genera of seed plants in China (Wu 1965, 1991), in which fifteen areal-types or floristic elements were recognized. This scheme has been widely used in analyzing national, regional floras of China at various levels and proved helpful in understanding biogeographic issues, such as endemism, vicarism and disjunctive distributions. As floristic data accumulated with the completion of FRPS and progress of FOC, the scheme was modified and elucidated, and enlarged to include distribution patterns or areal-types of families of seed plants of the world, in which eighteen types were recognized (Wu et al. 2003b; Wu et al. 2006b). 8
9 Although China is nearly identical in size compared to the United States, the vascular plant flora of China is much richer than that of the USA (Guo and Ricklefs 1998). China is also the only country in the world with an unbroken latitudinal gradient of tropical, subtropical, temperate and boreal forests. This, together with the complexity of mountain ranges and active tectonic movement made it possible for many living fossil plants to survive during clime change in the Miocene and the Pleistocene glaciations. China is therefore referred as an important center of survival (or museum ) (Axelrod et al. 1998). Wu & Wu showed that as many as 30 families of seed plants are endemic to Eastern Asia, and more than 600 genera are endemic (more than twice as many as those estimated by Takhtajan (1978). The endemism of the Chinese flora at the generic level was discussed in detail (Ying et al. 1993). The distribution patterns of 52 taxa (families, subfamilies, tribes or genera) of Chinese seed plants were elucidated (Lu 1999). By analyzing the floristic data, the Eastern Asiatic Floristic Kingdom was considered as an important center of speciation and evolution (or cradle ) for seed plants (Wu and Wu 1998; Qian 2002). An analysis of the 239 endemic genera in 67 families of seed plants in China showed that there are five families containing morn than ten endemic genera, i.e., Gesneriaceae (27, number of endemic genera), Compositae (20), Labiatae (12), Cruciferae (11), and Umbelliferae (10), and 15 other families with two endemic genera, and other 30 families with only one endemic genus. Four monotypic families, i.e., Ginkgoaceae, Davidiaceae, Eucommiaceae and Acanthochlamydaceae, are the most ancient, relic and characteristic in the flora of seed plants in China. In angiosperms, the endemic genera are mostly relic, and are represented in all lineages in the eight-class system of classification of angiosperms, and endemism can be found in almost every evolutionary stage of extant angiosperms (Wu et al. 2005). Molecular Phylogenetics and Biogeography In the past ten years, advances in molecular biology and biotechnology greatly shaped the development of other disciplines of life sciences with no exception. Application of molecular approach to address phylogenetic, biogeographic and ecological issues resulted in the birth of molecular phylogenetics, molecular biogeography and phylogeography, as well as molecular ecology. Molecular phylogenetic and biogeographic studies of angiosperms in China also witnessed a progressive development. Zhang and Ge (2007) summarized the advances in 9
10 molecular evolutionary studies in the past decade in China, including some advances in plant molecular biogeography above the species level, such as the Betulaceae (Chen et al. 1999) and the Pinaceae (Wang et al. 2002). Another interesting example is the Saururaceae, a family disjunctively distributed in Eastern Asian and eastern North America. Analysis of sequence data of five loci of three genomes revealed that the Eastern Asian Houttuynia is sister to the North American Anemopis (Meng et al. 2003). This was also suggested by analysis based on morphological data (Wu 1983). However, previous morphogical cladistic analysis did not support that the clade composed by Houttuynia and Anemopsis was the basal one in the family (Tucker et al. 1993). A re-examination of the ontogenetic data suggested that the coding of the primordia of the stamens in the previous analysis was wrong. Using the corrected matrix, the result of the morphological analysis was the same as that of molecular tree (Meng et al. 2003). Indeed, molecular phylogenies revealed some important results, particularly in the Eastern Asia- North American disjunct distribution (Xiang et al. 1998; Wen 1999). The combination of morphological, molecular and fossil data made it possible to date the divergence time of the floristic disjunction (Xiang 2000). A collective study on ten genera of the disjunction by a group of Chinese American botanists using molecular data supported the hypothesis that Eastern Asia is a cradle of diversity for most of the disjunct genera (Xiang et al. 2004). Recently population genetic or phylogenetic study on Tacca (Dioscoreaceae) and Taxus (Taxaceae) also verified the Tanaka-Kaiyong line (Li and Li 1997), an important biogeographic line in Eastern Asia (Zhang et al. 2006; Gao et al. 2007). Concluding Remarks The FRPS and the nearly-completed FOC provide a base for in-depth floristic analysis, phylogenetic and biogeographic study of plants in China. The integration of morphological and molecular data, together with fossil evidence is changing the face of plant phylogenetics and biogeography. The discovery of the earliest angiosperms, Archaefructaceae and Hyrcantha in Northeast China (Sun et al. 2002; Dilcher et al. 2007) is also verifying the point of view made by C. Y. Wu and colleagues that Eastern Asia is an important centre of diversification of angiosperms. However, to reach a sound conclusion, more fossil material should be uncovered and studied in the light of modern biology in China and adjacent areas. 10
11 In the past three or four years, progress in genomics in Arabidopsis thaliana (Cruciferae), Oryza sativa (Gramineae), Populus trichocarpa (Salicaceae), Vitis vinifera (Vitaceae) and Zea mays (Gramineae) provides great opportunity for phylogenetists and biogeographers. Based on the floristic data accumulated in the past ten years and information and methodology developed in the genomic era, it is hoped that the study of plant phylogenetics and biogeography in China and elsewhere will provide solid evolutionary basis for plant diversity conservation and sustainable use of plant resources in the next decade. Acknowledgements I am very grateful to the editorial committee, particularly S. C. Chen (CAS Institute of Botany) for the earlier history of the FRPS. I also thank the editorial center at Missouri Botanical Garden, particularly Lisa Pepper for the newest statistics of the FOC treatments. Stephen Blackmore (Royal Botanic Garden Edinburgh), Qin-Er Yang (FOC co-director, currently CAS South China Institute of Botany) and an anonymous reviewer are thanked for their critical reading of earlier versions of the manuscript. Lulu Huang (CAS Kunming Institute of Botany) provided valuable assistance to the reference list by using EndNote. References APG (1998). An ordinal classification for the families of flowering plants. Ann. Missouri Bot. Gard. 85, APG-II (2003). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141, Axelrod DI, Al-Shehbaz I, Raven PH (1998). History of the modern flora of China. In: Zhang AL, SGW, eds. Floristic Characteristics and Diversity of East Asian Plants. China Higher Education Press & Springer_Verlag, Beijing & Berlin. pp Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD et al. (1993). Phylogenetics of Seed Plants: An Analysis of Nucleotide Sequences from the Plastid Gene rbcl. Ann. Missouri Bot. Gard. 80, Chen ZD, Manchester SR, Sun HY (1999). Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology, and paleobotany. Am. J. Bot. 86, Ching RC (1959). Flora Reipublicae Popularis Sinicae. Vol. 2 (Pteridophytes (1)). Science Press, Beijing. Cronquist A (1981). An Integrated System of Classification of Flowering Plants. Columbia University Press, New York. 11
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15 15
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