Bot. Rev. (2010) 76:346–376 DOI 10.1007/s12229-010-9055-7

Seed Plant Endemism on Hainan Island: A Framework for Conservation Actions

Javier Francisco-Ortega1,2 & Zhong-Sheng Wang3,12 & Fa-Guo Wang4 & Fu-Wu Xing4 & Hong Liu2,5 & Han Xu6 & Wei-Xiang Xu3 & Yi-Bo Luo7 & Xi-Qiang Song8 & Stephan Gale9 & David E. Boufford10 & Mike Maunder1,2,11 & Shu-Qing An3,12

1 Department of Biological Sciences, Florida International University, Miami FL33199, USA 2 Center for Tropical Plant Conservation, Fairchild Tropical Botanic Garden, Coral Gables, Miami, FL 33156, USA 3 Laboratory of Forest Ecology and Global Change, School of Life Science, Nanjing University, Nanjing 210093, People’s Republic of China 4 South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, People’s Republic of China 5 Department of Earth and Environment, Florida International University, Miami FL33199, USA 6 Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520, People’s Republic of China 7 Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing 100093, People’s Republic of China 8 Key Laboratory of Tropical Horticultural Plant Resources and Genetic Improvement, Hainan University, Haikou 570228, People’s Republic of China 9 Kadoorie Farm and Botanic Garden, Lam Kam Road, Tai Po, New Territories, Hong Kong SAR, People’s Republic of China 10 Harvard University Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA 11 Al Ain Wildlife Park and Resort, PO Box 1204, Al Ain, Abu Dhabi, United Arab Emirates 12 Authors for Correspondence; e-mail: [email protected]; [email protected]

Published online: 20 May 2010 # The New York Botanical Garden 2010

Abstract Hainan, the second largest island of China, has the most extensive and best preserved tropical forests of this country. A network of 68 protected areas (54 of them are terrestrial) provides in situ conservation for the unique ecosystems of the island. We: (1) discuss an updated check-list of seed-plant species that are endemic to Hainan, (2) evaluate the extent to which the endemic flora has been the subject of molecular studies, and (3) investigate the conservation status of these species. We recognize 397 endemic species on the island, 271 of which are reported in the protected areas, and 144 of which have been Red-Listed (85 assigned to the Critically Endangered (40) or Endangered (45) IUCN categories). The families with the highest number of endemics are Rubiaceae (33 species), Lauraceae (27 species), and Poaceae (26 species). The island has only seven endemic genera, all of which are unispecific. Compared with other tropical islands, Hainan has a low number of endemics but our preliminary observations suggest that the island has a highly disharmonic flora when compared with that from the mainland. Nevertheless, most of the major clades of the seed-plant tree of life with representatives in China also have endemic species on the island. We argue that the low levels of endemism reflect Seed plant endemism on Hainan Island 347 the continental nature of Hainan and the fact that several areas of the island have not been fully inventoried. We were unable to find a single molecular systematic study focusing exclusively on the Hainan endemics; however, 24 of the endemic species have been included in phylogenetic studies targeting particular genera or families. Future research/conservation actions for the endemic flora of Hainan should focus in developing: (1) a red-list that assesses all 397 endemic species, (2) comprehensive floristic studies for the protected areas, (3) molecular phylogenetic and conservation genetic studies with a primary focus on the endemics, (4) studies to understand what ecological interactions are important in the biology of the endemic species, and (5) eco-geographical studies to identify Important Biodiversity Zones of endemism within Hainan and therefore potential new protected areas.

Keywords Asia . DNA Systematics . Angiosperms . Gymnosperms . Indo Burma Biodiversity Hotspot . Tropical botany

Introduction

Hainan: Physical and Ecological Features

Hainan, with an area of approximately 33,900 km2, is the second largest island of China (Fig. 1). It is located at the same latitude as northern Vietnam, and is only 24 km from the Leizhou Peninsula, Guangdong Province. Because of the relatively shallow waters of the Qiongzhou Strait (maximum depth of 120 m) (Cheng et al., 2008), it is likely that the island has been successively connected with and separated from the mainland during the recent Quaternary glacial and inter-glacial periods (Long et al., 2006). Hainan and its surrounding islands are the southernmost territory of the People’s Republic of China; therefore, it is the region of this country with the strongest tropical influence. Accordingly, some authors have argued that the flora of Hainan and other areas of southern China should be placed within the Indo-Malesian floristic subkingdom (Zhu & Roos, 2004). Hainan has a complex geological origin, greatly determined by the expansion of the South China Sea Basin and by tectonic interactions between the Eurasian, Philippine and Indian plates (Liu et al., 2008). The island is volcanically active and sits on a geological hotspot or mantle plume (Zhao, 2007); the latest volcano eruptions took place in 1883 and 1933 at Lingao and Chengmai counties, respectively (Liu, 1999). Geologically, Hainan was originally part of two different blocks of Gondwana that merged with Eurasia during the Late Permian to Middle Triassic (Cai & Zhang, 2009). Previous studies claim that the island began to separate from the mainland along a fault-line that developed in the Qiongzhou Strait during the Quaternary (Wang et al., 1995a; Xing et al., 1995; Zhao et al., 2007; Yao et al., 2009). However, results of tectonophysical and marine sediment studies suggest that Hainan began to split from the mainland much earlier, during the Tertiary. The Qiongzhou Strait is located on the eastern margin of the Beibuwan Basin (Fig. 1), and it is believed that this submerged geological depression developed in the late Cretaceous or Tertiary (Ren et al., 2002). Additional support for a pre-Quaternary origin comes from the 348 J. Francisco-Ortega et al.

Fig. 1 Map of Hainan Island and southern portion of Leizhou Peninsula showing location of four protected areas (coded 1 = Bawangling; 2 = Diaoluoshan; 3 = Jianfengling; 4 = Yinggeling) discussed in our review presence of massive Tertiary marine sediments in the Qiongzhou Strait (Li et al., 2008; K.-J. Zhang, pers. comm.). Seismic studies undertaken by Peng (2000) support an Oligocene origin for Hainan, suggesting that marine erosion played a major role in its insular origin. In addition, these seismic data do not support the existence of any major geological fault along the strait (Peng, 2000). Seed plant endemism on Hainan Island 349

The complex geology of Hainan has resulted in an environment that includes volcanic rocks in the northern region, granitic and metamorphic rocks mostly in the center, south and southeastern sectors, and limestone deposits primarily confined to the southwestern corner of the island (Zhou et al., 1999; Li et al., 2000; Xing et al., 2004; Ding et al., 2005; Qin et al., 2005; Lei et al., 2009). The northern portion of Hainan has an overall elevation of 300 m and is relatively flat. In contrast, the southern and central regions have a highly dissected topography. Wuzhi Shan (1,876 m), the highest mountain, is located in the center of the island. Approximately 39% of Hainan is covered by mountains and hills, including at least 87 peaks with an altitude of more than 900 m (Hsieh & Zhong, 1990). Hainan has a tropical climate dominated by the summer monsoon with a dry season extending between November and April and a rainy season between May and October. The average annual rainfall is over 1,600 mm, but this is not evenly distributed because of the orography of the island. The eastern section of the island receives an annual average precipitation of 2,000–2,400 mm whilst in the western sector this value is reduced to 1,000–2,000 mm (Hsieh & Zhong, 1990). During the rainy season, the island is in the path of typhoons (Wu et al., 2007; Wang et al., 2008). Because of its varied topography and uneven distribution of rainfall, the vegetation of Hainan, which has been severely influenced by human activities (see below), is rich and varied. Currently, the plant communities of Hainan survive in a highly fragmented landscape that includes natural areas, human settlements, and farmland (Wang et al., 2007a). The western semi-arid region has the only tropical savannas in China (Li et al., 2007). Tropical monsoon forests with evergreen and deciduous elements also exist in this region and in the lowlands of southern Hainan (Wang et al., 2007a). Most of the remaining natural vegetation is primarily composed of lowland or montane seasonal evergreen rainforests (Wang et al., 1995a, 2007a). At higher elevations (above 1,300 m) are elfin and tropical evergreen forests where lichens, mosses, small trees/shrubs, and conifers dominate (Wang et al., 1995a, 2007a; Ouyang et al., 2001). The coastal areas include mangroves, xerophytic thorn scrub, forests over sand, and seasonal evergreen forests (Huang et al., 1995; Wang et al., 2007a). In addition, Hainan has some small patches of tropical bamboo forests, mostly located in the central and southern parts of the island (Wang et al., 2007a).

Hainan Biota: A Major Conservation Priority in Asia

Hainan is the largest island of the Indo Burma Biodiversity Hotspot and has the best preserved and most extensive tropical forests in China (Deng et al., 2008; Zang & Ding, 2009). The island is the site of the Hainan Island Monsoon Rain Forest Ecoregion, one of the 26 terrestrial habitats of China internationally recognized by the World Wildlife Fund for its global ecological importance. In addition, its coastal plains are part of the South China–Vietnam Subtropical Evergreen Forests Ecoregion. Hainan has been a major focus for international conservation as it harbors a unique vertebrate fauna, including one of the most critically endangered apes (the Hainan Black-Crested Gibbon (Chan et al., 2005b; Geissmann & Chan, 2004; Zhou et al., 2005)), the Hainan Eld’s Deer (Zeng et al., 2005), the poorly 350 J. Francisco-Ortega et al. known Hainan gymnure (Stone, 1995), and five endemic species of birds (Chen, 2008). Three of the bird endemics (the Hainan Partridge, the Hainan Leaf Warbler, and the White-eared Night-heron) have a restricted distribution and are of conservation concern (Chan et al., 2005a; IUCN, 2009). Accordingly, Hainan has been identified by BirdLife International as an Endemic Bird Area (EBA 142) (Chan et al., 2005a), and the mangroves of Dongzhaigang, located in the north-eastern extreme of the island, have been designated a Wetland of International Importance by RAMSAR (2009). The relevance of Hainan as being of national priority for conservation has been recognized by the Chinese Government as well. The southern half of the island has been officially declared one of the eleven Critical Terrestrial Regions for Biodiversity in China (Compilation Group of China’s Biodiversity, 1998) and it is listed among the 33 Priority Conservation Areas of China (Terrestrial Part) (Xie et al., 2009). Conservation concerns also extend to plants, and a recent study on distribution of endangered species in China identifies southern Hainan as one of eight hotspots for plant conservation in the country (Zhang & Ma, 2008). Additionally, the Tropical Forests of Hainan Island (CPD Site EA27) is one of 41 Centres of Plant Diversity identified for China by the World Wildlife Fund and the IUCN, World Conservation Union (Wang et al., 1995b). The original ecosystems have seen major declines during the last 100 years. By the 1950s approximately 25.5% of Hainan was covered by forests, but by 1998 this figure had decreased to 8.7% (Compilation Group of China’s Biodiversity, 1998). Large forest areas have been replaced by rubber plantations (∼5,100 km2 by 2006) and other forms of agriculture, as well as industrial and urban developments (Guo et al., 2006; Wang et al., 2007a). The large reduction in forest cover led to drastic actions by governmental agencies, including a logging ban in 1993 (Zang & Ding, 2009), reforestation, mostly with fast-growing species of trees such as eucalyptus (Zhang et al., 2000), and the establishment of a network of nature reserves to protect the remaining patches of original forest (Compilation Group of China’s Biodiversity, 1998; Ouyang et al., 2001; Zheng & Zhu, 2004). By the end of 2008, Hainan had 68 protected areas, of which 54 are terrestrial, representing approximately 5.4% of the territory (Ministry of Environmental Protection of People’s Republic of China, 2008). This system of reserves includes 100% of the remaining forests. However, major conservation challenges remain because of actual and potential conflicts between environmental protection policies and the rapid economic development that Hainan has experienced since 1988, when the island was declared a Special Economic Zone (SEZ) (Caldecott, 1996). These conflicts are likely to increase in the future as recent projections anticipate a significant increase in demand for natural resources throughout China for the first half of the 21st century (Dong et al., 2008; Grumbine & Xu, 2009). In the last 20 years Hainan has experienced major developments in the mining and tourism industries. The island has abundant geological resources and at least 63 exploitable minerals (including oil, gas, and coal) have been identified (Anonymous, 1998). Since the 1950s, mining has been the main heavy industry of Hainan (Feng & Goodman, 1995). Indeed the island has the largest iron ore mine (Hsieh & Zhong, 1990; Fosun International, 2009) and the largest reserves of titanium and zircon in Seed plant endemism on Hainan Island 351

China (Feng & Goodman, 1995). Hainan harbors the largest, but least industrialized, SEZ of China, and has a growing population of over 8,300,000 inhabitants (Liu, 2009). The island, however, has followed the rest of the country in the fast trend for development. Between 1987 and 2002 the gross domestic product of Hainan increased 11 fold (Liu, 2009). Such remarkable growth has prompted rapid urbanization, the establishment of new tourist resorts and building projects along coastal areas, as well as new infrastructure including major road systems and two major international airports (Feng & Goodman, 1995; Stone & Wall, 2003;Gu& Wall, 2007).

Hainan Endemic Flora: Conservation Unknowns—Review Objectives

The latest checklist of the seed plants of Hainan was published fifteen years ago (Wu et al., 1994). Since then, three additional studies have reviewed plant endemism and phytogeographical patterns on the island (Wang et al., 1995a; Xing et al., 1995; Zhang, 2001). None of these recent studies, however, have provided a checklist of the endemic species. Between 1964 and 1977 a full account for the flora was published in the four volumes of Flora Hainanica (Chun et al., 1964;Chun& Chang, 1965; Institute of Botany of Guangdong Province, 1974, 1977). Addition- ally, Ko (1989) reviewed phytogeographical links between Hainan and neighboring regions, and the plants of the island are covered in the 82 volumes of the Flora Reipublicae Popularis Sinicae (between 1959 and 2003) and in the 16 volumes of the Flora of China published so far. However, these previous studies show disparate figures for the number of endemic species, ranging from 395 (Ko, 1989) and 505 (Xing et al., 1995) for seed plants, to 630 (including all vascular plants) (Wang et al., 1995a). A more recent checklist developed by the authors of this review is presented in a separate paper in this issue of Botanical Review (Francisco-Ortega et al., 2010). Floristic lists are available for four of the protected areas of Hainan: Bawangling, Diaoluoshan, Jianfengling, and Yinggeling (Zeng et al., 1995; Kadoorie Farm & Botanic Garden, 2001; Jiang et al., 2006a; Bawangling National Nature Reserve, unpublished; Yinggelin Nature Reserve, unpublished), and although we are aware that all of the remaining natural forests of Hainan are currently officially protected, it is uncertain to what extent the endemic flora of the island is being preserved within this in situ conservation network. Since no comprehensive red list for the endemic flora of Hainan based on the IUCN (2001) conservation categories exists, the component of the endemic flora needing conservation action is uncertain. Unknown factors concerning the conservation status of Hainan endemics also extend to their distribution patterns. The island has a complex geology and highly dissected topography. Recent floristic studies focusing on the limestone areas of Hainan (Wang et al., 2006, unpublished) show that at least 15 of the endemics are restricted to this section of the island (Appendix 1). However, there are no comprehensive floristic data for those areas of the island dominated by metamorphic, plutonic, or volcanic rocks. Likewise, there is a need for local endemism studies focusing on the main vegetation zones of Hainan and on those areas with inaccessible topography. 352 J. Francisco-Ortega et al.

An understanding of the distribution patterns and conservation status of the Hainan endemics could guide future plant conservation action. In this study we discuss our updated checklist of the seed plants endemic to Hainan Island (Francisco- Ortega et al., 2010), as well as a preliminary overview of the conservation status of these endemic species. It is widely recognized that phylogenetic studies can provide an evolutionary perspective for biodiversity conservation (Rodrigues et al., 2005; Sinclair et al., 2005); therefore, we also reviewed molecular phylogeny studies that have included Hainan endemics. The main goal of this paper is to provide a baseline framework for those directly involved in conserving the unique plant heritage of Hainan. We hope that this study will encourage additional biological and ecological studies of Hainan’s endemic flora.

The Endemic Flora of Hainan

Taxonomic Overview and Global Significance

Based on our studies (Francisco-Ortega et al., 2010) the endemic flora of Hainan comprises 397 species of seed-plants in 215 genera and 74 families (Table 1). This represents approximately only 3% of the total endemic flora of China (which is estimated to be at least 12,000 species, N. Turland, pers. comm.) and only 12% of the native flora of Hainan (approximately 3,315 species, Xing et al., 1995). The Hainan endemics belong to 12 of the major lineages of the tree of life of seed plants (Soltis et al., 2005) (Figs. 2 and 3). Only four of the lineages with endemics in China (i.e., Austrabaileyales, Caryophyllales, Chloranthales, and Sabiales) do not have any species endemic to Hainan. The vast majority of the Hainan endemics (269) belong to the Eudicot clade. Only five species of gymnosperms are endemic. Eleven families have more than nine endemic species each, and these account for 53% of the total endemic flora (Table 2). Rubiaceae (33 spp.), Lauraceae (27 spp.), Poaceae (26 spp.), Orchidaceae (23 spp.), and Fagaceae (23 spp.) have the highest number of endemic species (Table 2). Hainan is considered a major biodiversity center for bamboos in the Asia-Pacific region (Bystriakova et al., 2003) therefore it is not surprising that 19 of the endemic members of the Poaceae are placed in seven genera of Bambuseae (Table 1). Only seven genera are endemic to the island. All are unispecific and therefore represent only 3% of the total endemic flora (Table 3). The ten genera with the highest number of endemic species have more than five species each, together contributing 79 species (19%) to the total endemic flora. Of these, Hedyotis (11 spp.), Bambusa (10 spp.), and Syzygium (9 spp.) are the most species- rich (Table 4). Four of these endemic-rich genera (i.e., Beilschmiedia, Castanopsis, Hoya,andHedyotis) have a large proportion (between 21 and 30%) of their China endemics restricted to Hainan (Table 4). Almost half of the genera (97) with endemic species in Hainan are species-rich (more than 99 species) elsewhere (Table 1).Nineofthegenerahaveatleast20% of their taxonomic diversity represented by species endemic to Hainan (Table 5). In particular, Hainan endemics comprise 67% of the total species richness of both Chuniophoenix and Seed plant endemism on Hainan Island 353

Table 1 Geographical Distribution and Taxonomic Diversity of Genera With Endemic Species on Hainan

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Acanthaceae, Asterids Cosmianthemum 1/3 9 Tropical E Asia Bremekamp Peristrophe Nees 1/2 25 Tropical and subtropical Africa and Asia Staurogyne Wallich 4/8 110 America, Africa, tropical Asia Annonaceae, Magnoliales Artabotrys R. Br. 2/4 100 Paleotropical Chieniodendron Tsiang 1/1 1 Hainan Island &P.T.Li Fissistigma Griffith 1/7 60 E India to NE Australia Apocynaceae, Asterids Cosmostigma Wight 1/1a 3 Tropical and subtropical Asia Gymnema R. Br. 1/4 25 Tropical and subtropical Asia, S Africa, Oceania Hoya R. Br. 6/20 100 SE Asia, Oceania Kopsia Blume 1/1 20 SE Asia Pentastelma Tsiang & 1/1 1 Hainan Island P. T. Li Rauvolfia L. 1/1 70 Tropical Asia, Africa, America, Madagascar Toxocarpus Wight & 3/7 40 Tropical Asia, Africa, Pacific islands Arn. Tylophora R. Br. 2/24 60 Tropical and subtropical Asia, Africa, Australia Aquifoliaceae, Asterids Ilex L. 6/149 600 Tropical and subtropical to temperate regions of both the N and S hemispheres Araceae, Monocots Arisaema Mart. 1/61 150 E and SE USA, N Mexico, E and NE Africa, Arabia, temperate E Asia, tropical S, SE, and E Asia, Indonesia Homalomena Schott 1/2 110 S and SE Asia to Melanesia, tropical America Schismatoglottis Zoll. & 1/1 120 SE Asia to New Guinea, N South America Moritzi Araliaceae, Asterids Dendropanax Decne. & 1/7 80 Tropical America, E and SE Asia Planch. Heteropanax Seem. 1/2 6 E, S, and SE Asia Macropanax Miq. 1/5 15 E, S, and SE Asia Arecaceae, Monocots Calamus L. 4/21 374 From tropical Africa through S Asia to SE Pacific Chuniophoenix Burret 2/2 3 China, Vietnam Licuala Thunb. 1/2 134 From S Asia to SW Pacific Aristolochiaceae, Piperales Aristolochia L. 3/33 400 Europe (mainly Mediterranean), tropical Africa (including Madagascar, tropical Asia, Japan, the Philippines, New Guinea, N Australia 354 J. Francisco-Ortega et al.

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Thottea Rottb. 1/1a 25 Deccan peninsula, SE Asia, Sri Lanka, the Philippines, Sunda Islands Asparagaceae, Monocots Disporum Salisb. ex 1/8 20 Bhutan, China, India, Japan, SE Asia D. Don Asteraceae, Asterids Calotis R. Br. 1/1a 29 Mostly Australia, SE Asia Sinosenecio B. Nord. 1/35 40 SE Asia, mostly China, Canada Strobocalyx Sch. Bip. 1/3 9 SE Asia, India, S China, Vietnam, Malaysia, Indonesia Balanophoraceae, Santalales Balanophora L 1/1 19 Mostly tropical Africa and Australia, temperate to tropical Asia, Pacific islands Balsaminaceae, Asterids Impatiens L. 1/187 1,000 Tropical and subtropical mountains of the E hemisphere, some species in temperate Asia, Europe, and North America Begoniaceae, Rosids Begonia L. 4/184 1,400 Tropics and subtropics Boraginaceae, Asterids Ehretia P. Browne 2/7 50 Mostly in Africa and S Asia, a few in N America and the Caribbean Buxaceae, Buxales Buxus L. 2/15 100 C America, West Indies, Africa, Madagascar, E Asia Campanulaceae, Asterids Lobelia L. 1/9 400 Cosmopolitan Capparaceae, Rosids Capparis L. 2/10 250 Pantropical with outliers in the subtropics and the Mediterranean Caprifoliaceae, Asterids Lonicera L. 1/62 200 N America, Europe, Asia, N Africa Celastraceae, Rosids Euonymus L. 2/50 130 Old and New World World, Australia Glyptopetalum Thwaites 1/7 20 Tropical and subtropical Asia Gymnosporia (Wight & 1/7 80 Tropics and Subtropics of both the Old and Arn.) Hook.f. New Worlds, but mainly tropical Africa and Asia Maytenus Molina 2/6 200 Tropics and subtropics of both the Old and New Worlds Microtropis Wall. ex 1/20 66 Tropics and subtropics of SE Asia, Africa, and Meisn. the New World Salacia L. 3/8 200 Tropics of New and Old World, Australia Connaraceae, Rosids Ellipanthus Hook.f. 1/1a 13 Mostly SE Asia, also in tropical E Africa and Madagascar Seed plant endemism on Hainan Island 355

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Convolvulaceae, Asterids Erycibe Roxb. 1/4 67 Mostly tropical Asia, Australia, Japan, Malesia Cycadaceae, Gymnosperms Cycas L. 3/10 100 Mostly Indo-Chinese and Australian. Also in Malesia, Japan, India, Micronesia, Polynesia, Madagascar and E Africa Cyperaceae, Monocots Carex L. 3/280 2,000 Cosmopolitan Fimbristylis Vahl 2/15 300 Pantropical to (warm-) Temperate, mostly in SE Asia, Malesia, and NE Australia Hypolytrum Rich. 2/2a 40 Pantropical, mainly equatorial Lipocarpha R. Br. 1/3 35 Mostly pantropical Machaerina Vahl 1/2 50 Madagascar, SE Asia, Malesia, SE Australia, New Zealand, New Caledonia, Pacific islands to Tropical S America and the West Indies Mariscus Scop. 2/2 200 Tropics and subtropics Scirpus L. 2/6 20 Holartics, SE and E Asia, Malesia, SE Australia, Andean S America Dioscoreaceae, Monocots Dioscorea L. 1/21 600 Tropical and temperate regions Ebenaceae, Asterids Diospyros L. 8/42 550 Pantropical and extending into temperate regions Elaeocarpaceae, Rosids Sloanea L. 1/7 110 Tropics and subtropics Ericaceae, Asterids Vaccinium L. 1/51 450 Throughout the N hemisphere, also in the mountains of tropical Asia and C and S America, a few species in Africa and Madagascar Eriocaulaceae, Monocots Eriocaulon L. 4/16 400 Tropics and subtropics but mostly in Asia Euphorbiaceae, Rosids Acalypha L. 2/7 450 Pantropical Croton L. 4/15 800 Tropics and Neotropics but mostly in the New World Drypetes Vahl 1/2 200 Tropical and subtropical Africa, America, and Asia Euphorbia L. 1/11 2,000 Cosmopolitan Leptopus Decne. 1/3 10 From the Caucasus through India to China, Indonesia, and tropical Australia Mallotus Lour. 1/7 150 Tropical and Subtropical Asia, a few species in Africa and Australia Phyllanthus L. 3/4 800 Tropics and subtropics Trigonostemon Blume 1/1 60 From India to China, New Guinea, NE Australia, and New Caledonia Fabaceae, Rosids Christia Moench 1/1 10 India to China, Malesia and Australia 356 J. Francisco-Ortega et al.

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Crotalaria L. 3/5 690 Africa, Madagascar, tropical Asia, Australia, S, N, and C America Dalbergia L. f. 3/9 250 Pantropical, centered in the Old World Derris Lour. 1/11 60 Mainly Asia extending to E Africa, Australia, and W Pacific Indigofera L. 1/43 700 Mostly Pantropical Paraderris (Miq.) R. 1/2 13 Asia Geesink Sophora L. 1/9 50 SE Europe to W, C, and E Asia, Australia Fagaceae, Rosids Castanopsis (D. Don) 8/34 120 S and SE Asia Spach Cyclobalanopsis Oerts. 8/47 150 Mostly tropical and subtropical Asia Lithocarpus Blume 6/69 300 Asia Quercus L. 1/15 300 N Africa, Asia, Europe, N America, NW S America Gesneriaceae, Asterids Cathayanthe Chun 1/1 1 Hainan Island Chirita Buch.-Ham. ex 1/93 140 From the Western Himalaya and E and S China D. Don To S India and W Malesia Metapetrocosmea W. T. 1/1 1 Hainan Island Wang Oreocharis Benth. 2/26 28 C and S China, Vietnam, Thailand Paraboea (C. B. Clarke) 2/11 90 S China, Indonesia, Malesia, the Philippines Ridl. Hamamelidaceae, Saxifragales Chunia H. T. Chang 1/1 1 Hainan Island Distyliopsis Endress 1/4 6 S China, Taiwan, Malesia to New Guinea Hydrangeaceae, Asterids Dichroa Lour. 1/4 12 Mainly in E Asia and adjacent islands Icacinaceae, Asterids Nothapodytes Blume 1/6 7 Tropical Asia, reaching into temperate regions of China Platea Blume 1/1 5 Tropical Asia Juglandaceae, Rosids Engelhardia Lesch. ex 1/1 7 S and SE Asia, N India, the Philippines Blume Lamiaceae, Asterids Callicarpa L. 2/33 140 Mainly in tropical and subtropical Asia, a few in tropical America and Africa, and very few in temperate Asia and N America Gomphostemma Wall. ex 1/8 36 SW China, India to SE Asia, Malesia, and Benth. Indonesia Premna L. 1/31 200 Old World Tropics and subtropics Scutellaria L. 1/77 360 Worldwide, but only a few in tropical Africa Wenchengia C. Y. Wu & 1/1 1 Hainan Island S. Chow Seed plant endemism on Hainan Island 357

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Lardizabalaceae, Ranunculales Stauntonia DC. 1/18 25 From Burma to S China, Taiwan, S Japan Lauraceae, Laurales Actinodaphne Nees 2/13 100 Tropical and subtropical Asia Alseodaphne Nees 1/7 50 Tropical Asia Beilschmiedia Nees 7/33 300 Pantropical Cryptocarya R. Br. 4/15 250 Pantropical, centered in Malesia Dehaasia Blume 1/2 35 Asia, from S China to New Guinea, centered in Malesia Endiandra R. Br. 1/2 30 Asia, Australia, Pacific islands Lindera Thunb. 1/23 100 Mostly in Asia, also in N America and Australia Litsea Lam. 2/47 200 Tropical and subtropical Asia, Australia, N America to subtropical S America Machilus Nees 2/63 100 Tropical and subtropical S and SE Asia Neolitsea Merr. 3/35 85 Indo-Malesia to E Asia, a few in Australia Phoebe Nees 1/27 100 Asia Syndiclis Hook. f. 2/9 10 Bhutan, S China Lowiaceae, Monocots Orchidantha N. E. Br 1/2 10 S China, SE Asia, Indonesia, Malesia Magnoliaceae, Magnoliales Lirianthe Spach 1/5 12 SE Asia, China Magnolia L.b 1/1 20 C, E, and N America, including the Antilles Michelia L. 1/20 70 Tropical and subtropical Asia Malvaceae, Rosids Firmiana Marsili 2/5 16 Tropical, subtropical, and temperate Asia, also in Pacific islands Grewia L. 1/13 280 Africa. Madagascar, Indo-Malesia, China, Australia, W Pacific islands Reevesia Lindl. 3/12 25 Mostly in Asia: Himalaya, China, Malesia, a few in Mesoamerica Melastomataceae, Rosids Medinilla Gaudich. 1/5 375 Tropical Africa, Asia, and Pacific islands Melastoma L. 1/2 22 SE Asia, N Australia, Pacific islands Phyllagathis Blume 3/19 56 China, Indonesia, Malesia, SE Asia Scorpiothyrsus H. L. Li 2/3 3 China: Guangxi and Hainan Island Sonerila Roxb. 1/3 175 Tropical Asia Meliaceae, Sapindales Munronia Wight 1/3 4 Tropical and subtropical Asia Menispermaceae, Ranunculales Arcangelisia Becc. 1/1a 4 SE Asia Stephania Lour. 2/33 60 Tropical and subtropical Asia and Africa, a few in Oceania Tinospora Miers 1/3 32 SE Asia, Indo-Malesia to Australia and Pacific, a few in tropical Africa and Madagascar 358 J. Francisco-Ortega et al.

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Moraceae, Rosids Ficus L. 1/20 1,000 Mainly in Tropics and subtropics, particularly diverse in SE Asia Myrsinaceae, Asterids Ardisia Sw. 5/34 450 Tropical E and SE Asia, New World, Australia, Pacific islands Maesa Forssk. 2/13 150 Pantropical Myrtaceae, Rosids Decaspermum J. R. 4/5 30 SE Asia, Australia, Pacific islands Forst. & G. Forst. Syzygium Gaertn. 9/45 1,200 Tropical Africa, subtropical to tropical Asia, Australia, New Caledonia, New Zealand, Pacific islands Oleaceae, Asterids Chionanthus L. 1/3 60 Tropics and subtropics Jasminum L. 1/19 200 Old World Tropics and warm temperate regions Olea L. 2/8 40 Old World Tropics and warm temperate regions Orchidaceae, Monocots Anoectochilus Blume 2/7 40 India and the eastern Himalaya through S and SE Asia to Japan, Australia and SW Pacific islands Apostasia Blume 1/3 7 NE India, Nepal and Bhutan, north to S Japan, through SE Asia to New Guinea and N Australia Bulbophyllum Thouars 4/36 2,000 Tropics Ceratostylis Blume 1/1 100 From tropical Asia to New Guinea and the Pacific islands Crepidium Blume 2/5 280 From tropical Asia to Australia and the Indian Ocean Islands. Few species in temperate Asia Dendrobium Sw. 2/16 1,250 S Asia, Australia, New Zealand, Pacific islands Gastrochilus D. Don 1/16 38 India to SE Asia and Malesia, the Philippines, Japan Gastrodia R. Br. 1/8 16 S Africa, E Asia, Japan, Malesia, Australia, Pacific islands, New Zealand Liparis Rich. 3/16 320 Cosmopolitan but well represented in Tropics and subtropics of Asia and the New World, SW Pacific islands, and Australia Oxystophyllum Blume 1/1a 38 From SE Asia and Indonesia to the Philippines, New Guinea and Solomon Islands Phaius Lour. 1/4 40 Africa, Madagascar, tropical Asia, Malesia, NE Australia, SW Pacific islands, the Philippines Pinalia Lindl. 1/6 160 From NW Himalayas and NE India to Myanmar, S. China, Vietnam, Laos, Thailand, the Malay Archipelago, NE Australia, and the Pacific islands Sunipia Buch.-Ham. 1/1 27 From India, S China, and SE Asia to Taiwan ex Lindl. Seed plant endemism on Hainan Island 359

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Thrixspermum Lour. 1/3 100 Sri Lanka, Himalayan region but mostly in SE Asia Trichotosia Blume 1/1 50 From mainland Asia, through SE Asia to New Guinea and the Pacific islands Pentaphylacaceae, Asterids Adinandra Jack 3/17 80 E and SE Asia to Malesia Cleyera Thunb. 1/7 24 From Nepal to China, Korea, Japan,SE Asia, tropical America Eurya Thunb. 3/63 100 S China, SE Asia and nearby Pacific islands Ternstroemia Mutis ex 1/10 100 Tropical and subtropical Africa, America, Asia L. f. Pinaceae, Gymnosperms Keteleeria Carrière 1/3 5 Warm-temperate regions of China, Taiwan, Laos, and Vietnam Pinus L. 1/8 110 N hemisphere Piperaceae, Piperales Piper L. 3/34 1,000 Pantropical Poaceae, Monocots Ampelocalamus S. L. 1/12 13 From C Himalaya to S China Chen, T. H. Wen & G. Y. Shengc Bambusa Schreb.c 10/55 100 Tropical and subtropical Asia Bonia Balansac 1/4 5 S China, Vietnam Eragrostis Wolf 3/11 350 Tropics and subtropics Eulalia Kunth 1/5 30 Tropics of the Old World Fargesia Franch.c 1/77 90 China, E Himalaya, Vietnam Imperata Cirillo 1/1 10 Tropics and extending to warm Temperate regions Lingnania McClurec 2/10 14 S China, N Vietnam Oligostachyum Z. P. 3/15 15 China Wang&G.H.Yec Pogonatherum P. Beauv. 1/1 4 India to SE Asia, NE Australia, Polynesia Schizostachyum Neesc 1/6 50 SE Asia, China Setiacis S. L. Chen & Y. 1/1 1 Hainan Island X. Jin Polygalaceae, Rosids Polygala L. 3/21 350 Cosmopolitan Proteaceae, Proteales Heliciopsis Sleumer 1/2 10 SE Asia, Himalaya, China Ranunculaceae, Ranunculales Clematis L. 1/100 350 Widespread worldwide Rhamnaceae, Rosids Rhamnus L. 1/37 125 Widespread, absent only in Madagascar, Australia, and Polynesia Rosaceae, Rosids Prunus L. 1/3 30 Asia, Europe, N America 360 J. Francisco-Ortega et al.

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Rhaphiolepis Lindl. 1/4 15 SE Asia Rubus L. 1/139 250 Cosmopolitan Rubiaceae, Asterids Argostemma Wall. 2/4 100 W and W C tropical Africa, Tropical and subtropical Asia Benkara Adans. 1/4 19 SE Asia, China Ceriscoides (Hook. f.) 1/1a 11 Tropical Asia Tirveng Damnacanthus C. F. 1/6 13 Indo-China to temperate E Asia Gaertn Hedyotis L. 11/36 500 S China, Taiwan, tropical Asia, NW Pacific Lasianthus Jack 2/8 160 Panama, Caribbean, W, C and E tropical Africa, tropical and subtropical Asia, N Australia, SW Pacific Meyna Roxb. ex Link 1/1a 10 NE and E tropical Africa, Comoros, S China, tropical Asia Morinda L. 2/17 126 Tropics and subtropics Mussaenda L. 4/19 217 Paleotropics to S China Mycetia Reinw. 1/10 44 S China, tropical Asia Ophiorrhiza L. 2/47 316 India to S China and Pacific islands Psychotria L. 1/6 1,800 Tropics and subtropics Saprosma Blume 2/4 47 China, tropical Asia, SW Pacific Tarenna Gaertn. 1/12 203 Paleotropics to Pacific islands Wendlandia Bartl. ex 1/20 80 NE tropical Africa, tropical and subtropical DC. Asia, Australia Rutaceae, Rosidsa Clausena Burm. f. 1/5 30 Africa, E, S, and SE Asia, NE Australia, SW Pacific islands Melicope J. R. Forst. & 2/2 233 E, S, SE Asia, Australia, Indian Ocean Islands, G. Forst Madagascar, Pacific islands Salicaceae, Rosids Homalium Jacq. 1/10 200 Tropical regions of both hemispheres Populus L. 1/47 29 N hemisphere, from subtropical to boreal forests Salix L. 1/189 500 Mostly N hemisphere Santalaceae, Santalales Viscum L. 1/5 70 Temperate and tropical regions of the Old World Sapindaceae, Rosids Allophylus L. 2/2 200 Tropics and subtropics Lepisanthes Blume 3/4 24 Tropics of the Old World Mischocarpus Blume 1/1a 15 SE Asia to Australia Nephelium L. 1/1 22 SE Asia Paranephelium Miq. 1/1 8 Tropical Asia Sapotaceae, Asterids Madhuca Ham. ex 1/1 100 From India through Malesia and South China J. F. Gmel. to New Guinea Seed plant endemism on Hainan Island 361

Table 1 (continued)

Family, tree of life Number of endemic endemic Worldwide Worldwide distribution placement, and genus species in Hainan Island/ approximate approximate number of number of endemic species in China species (including Hainan)

Xantolis Raf. 1/3 14 From S India to Vietnam and S China and the Philippines Scrophulariaceae, Asterids Lindernia All. 1/12 100 Warm regions of New and Old World Smilacaceae, Monocots Heterosmilax Kunth 1/5 12 Tropical and subtropical Asia Stemonaceae, Rosids Stemona Lour. 1/5 27 Asia, Australia Symplocaceae, Asterids Symplocos Jacq. 3/18 250 Tropical and subtropical but absent in Africa Theaceae, Asterids Camellia L. 4/76 200 E Asia to Indomalaysia, mostly S China Polyspora Sweet 1/2 40 E and SE Asia Thymelaeaceae, Rosids Daphne L. 1/41 95 Europe, N Africa to India Wikstroemia Endl. 3/43 70 E and SE Asia to India, Australia, Hawaiian Islands, Pacific islands Urticaceae, Rosids Boehmeria Jacq. 1/6 80 Old and New World, mostly tropical and subtropical regions Pilea Lindl. 1/31 400 Worldwide in tropical, subtropical, and rarely in temperate regions Vitaceae, Rosids Cayratia Juss. 1/9 60 Tropical and subtropical Asia, Africa, Australia and the Pacific islands Leea L. 1/2 34 Mostly in Malesia, SE Asia, S and SW China and India, but also in Pacific islands, Australia, and Tropical Africa Tetrastigma (Miq.) 1/24 100 Tropical and subtropical Asia, a few in Planch. Australia Zingiberaceae, Monocots Alpinia Roxb. 2/37 230 Tropical and subtropical Asia, Australia, Pacific islands Amomum Roxb. 1/29 150 Tropical Asia and Australia a Genus has no native species in mainland China b The only species of Magnolia currently described for Hainan (M. bawangensis Y. W. Law, R. Z. Zhou & D. M. Liu) will need a new combination within Michelia if Xia et al. (2008) are followed in recognizing Magnolia as being restricted solely to the New World c Tribe Bambuseae

Scorpiothyrsus (Table 5). The vast majority of the genera (177, representing 83% of them) also have endemic species in the rest of China. The remaining 17% (38 genera with a total of 43 endemic species) do not have endemic species in either mainland China or Taiwan. Ten genera (with a total of 12 endemic species and 362 J. Francisco-Ortega et al.

Fig. 2 Phylogenetic arrangement of the 397 species of seed plants endemic to Hainan. Topology redrawn from Soltis et al. (2005). Lineages with endemic species in China are indicated with arrows. Numbers indicate number of species endemic to Hainan representing 5% of the genera) do not have species native to other parts of China (Table 1).

Historical Perspective

Approximately 37% of the endemic species (147 species) were originally described between 1930 and 1949. The majority of these (101 species) were described by Elmer D. Merrill (1876–1956) and Woon-Young Chun (1889–1971) (Fig. 4). Merril was one of the most important American taxonomists specializing in Asian plants (Howard, 1956). He was Director of the New York Botanical Garden between 1929 and 1935, and Director of the Arnold Arboretum between 1935 and 1946. Woon-Young Chun was one of the first Chinese botanists trained in the United States. He studied at Harvard University and, supported by the Sheldon Traveling Fellowship, he collected plants extensively on Hainan in 1919 (Madsen, 1999). In 1929 he founded the prestigious South China Botanical Garden (South China Botanical Garden, 2009), and between 1958 and 1977 he described 27 additional species from Hainan. A further 54 new endemic species were described for Hainan during the period 1973–1979 (Fig. 4). Twenty-six of these were published in the Flora Hainanica series. Interestingly, a small number of endemics were described in Flora Reipublicae Popularis Sinicae (four species) and in the Flora of China series (two species). However, the vast majority of endemics (286 species) were described in publications issued by Chinese institutes. Seed plant endemism on Hainan Island 363

Fig. 3 Selection of images of seed plant species endemic to Hainan. a Syzygium hainanense Hung T. Chang & R. H. Miao (Myrtaceae); b Stephania hainanensis H. S. Lo & Y. Tsoong (Menispermaceae); c Dendrobium sinense T. Tang & F. T. Wang (Orchidaceae); d Begonia peltatifolia H. L. Li (Begoniaceae); e Oreocharis dasyantha Chun (Gesneriaceae); f Hedyotis paridifolia Dunn (Rubiaceae); g Wenchengia alternifolia C. Y. Wu & S. Chow (Lamiaceae); h Impatiens hainanensis Y. L. Chen (Balsaminaceae). Photo credit: a–b Han Xu; c Xi-Qiang Song; d, g Rong-Tao Ling; e, f Xi-Long Zheng; h Xing-Sheng Qin 364 J. Francisco-Ortega et al.

Table 2 Families with More Than Nine Endemic Species Each

Family Number of endemic species Number of genera with endemic species

Rubiaceae 33 15 Lauraceae 27 12 Poaceae 26 12 Fagaceae 23 4 Orchidaceae 23 16 Apocynaceae 16 8 Cyperaceae 15 7 Euphorbiaceae 14 8 Myrtaceae 13 2 Fabaceae 11 7 Celastraceae 10 6 Total 211 (53a) 97 (45b) a Percentage of endemic species b Percentage of genera with endemic species

A cumulative analysis of the chronology of discovery of endemic species suggests that undescribed species are steadily being discovered and there is no sign of even approaching a final figure for the number of Hainan endemics (Fig. 4). Importantly, these results suggest that new botanical explorations and taxonomic revisions are likely to lead to the discovery of additional endemics for the island. Based on our field experience, it appears that some areas of Hainan need to be further explored, particularly areas with primary forest, such as those at Jianfengling, Yinggeling, Bawangling, Wuzhishan and Diaoluoshan. They should be regarded as priorities for further plant exploration (Kadoorie Farm & Botanic Garden, 2001, 2002). We expect that additional Hainan endemics will continue to be discovered as some of these more remote areas are explored and new taxonomic studies are undertaken.

Table 3 Genera of Seed Plants Endemic to Hainan

Genus Family Number of species

Chieniodendron Annonaceae 1 Pentastelma Apocynaceae 1 Cathayanthe Gesneriaceae 1 Metapetrocosmea Gesneriaceae 1 Chunia Hamamelidaceae 1 Wenchengia Lamiaceae 1 Setiacis Poaceae 1 Total (percentage of endemic species) 7 (2) Seed plant endemism on Hainan Island 365

Table 4 Genera with More Than Five Endemic Species Each

Genus Number of endemic Number of endemic species Worldwide number species on Hainana in China, including Hainan of species

Hedyotis (Rubiaceae) 11 (30) 36 500 Bambusa (Poaceae) 10 (18) 55 100 Syzygium (Myrtaceae) 9 (2) 45 1,200 Castanopsis (Fagaceae) 8 (23) 34 120 Cyclobalanopsis (Fagaceae) 8 (17) 47 150 Diospyros (Ebenaceae) 8 (19) 42 550 Beilschmiedia (Lauraceae) 7 (21) 33 300 Hoya (Apocynaceae) 6 (30) 20 100 Ilex (Aquifoliaceae) 6 (4) 149 600 Lithocarpus (Fagaceae) 6 (9) 69 300 Total (percentage of Hainan 79 (19) endemic species) a Values in parentheses represent percentage of total number of endemics in China

A Comparison with Other Tropical Islands and Disharmony

The situation in Hainan reflects that on other tropical islands, where most of the endemic genera are unispecific (reviewed by Francisco-Ortega et al., 2007). However, despite its relatively large size, Hainan has few endemics. For instance, Jamaica is approximately one third of the size of Hainan and yet it has at least three

Table 5 The Genera With Endemic Species That Have at Least 20% of Their Taxonomic Diversity on Hainan

Genus, family Number of Worldwide Worldwide distribution endemic species number of species

Chuniophoenix (Arecaceae) 2 2 China, Vietnam Scorpiothyrsus (Melastomataceae) 2 3 China: Guangxi and Hainan Island Cosmostigma (Apocynaceae) 1 3 Tropical and subtropical Asia Arcangelisia (Menispermaceae) 1 4 SE Asia Munronia (Meliaceae)a 1 4 Tropical and subtropical Asia Pogonatherum (Poaceae) 1 4 India to SE Asia, NE Australia, Polynesia Keteleeria (Pinaceae) 1 5 Warm-temperate regions of China, Taiwan, Laos, and Vietnam Bonia (Poaceae) 1 5 S China, Vietnam Platea (Icacinaceae) 1 5 Tropical Asia Total (percentage of endemic species) 11 (2) a Number of species follows Peng and Bartholomew (2008); however, Zhang et al. (2009) consider Munronia to have more than 17 species 366 J. Francisco-Ortega et al.

Fig. 4 Publication of original descriptions of the 397 seed plant species endemic to Hainan. Solid squares = total number of species described at particular yearly intervals; open circles = cumulative publications during the yearly intervals included in our study. Data refer to year of publication of basionym or to year when the species was first proposed in a taxonomic journal, even if the code of nomenclature in effect at the time was not followed times the number of endemic species (Adams, 1972). Likewise, Taiwan (35,800 km2) is slightly larger than Hainan but has approximately 1,000 endemic species (Hsieh, 2003). Other island systems much smaller than Hainan such as New Caledonia, the Hawaiian archipelago, and the Canary Islands also have a higher number of endemic species (Wagner et al., 1990; Santos-Guerra, 2001; Jaffré et al., 2004). The low level of endemism found in Hainan might be the result of the island’s close proximity to the mainland and the fact that it has been repeatly joined to the continent during recent glacial periods. Although the historical data (Fig. 4) suggest that new endemic species will be described from Hainan in the future, we anticipate that many will lose their endemic status as the floras of Vietnam and South China become better studied. In conclusion, our review clearly supports the view that the flora of Hainan is continental in nature, and that this is probably because of the island’s geographical proximity to the mainland and its geological and paleo- environmental histories. The low proportion of endemic species among the Asteraceae is striking, since this family is frequently cited for best exemplifying the paradigm of adaptive radiation on islands (Francisco-Ortega et al., 2008; Crawford et al., 2009). Likewise, although the Arecaceae are notable for their high rate of endemism on the Pacific islands (Morici, 2004), they have only seven species in three genera endemic to Hainan. Other genera have a few endemic species in Hainan but high levels of endemism in the rest of tropical China, among them there are Begonia and Impatiens (Chen et al., 2007;Ku et al., 2007). In contrast Cycas, a genus with over 11 insular endemic species in the Pacific Basin, has three endemics in Hainan. Apart from New Guinea, which also has three endemic species, no other island in the region has a higher number of endemic species (Laubenfels & Adema, 1998). There are also three endemic species of Cycas in the Philippines, but two of them occur on the island of Luzon, and the Seed plant endemism on Hainan Island 367 third one is restricted to the island of Palawan (Madulid & Agoo, 2009). Although we do not aim to make a full comparative study of the flora of Hainan with that of the closest source areas, the low level of endemism in Begonia and Impatiens and in the sunflower and palm families appears to support the disharmonic nature of the Hainan flora as compared with surrounding floras. Brigssia Craib (Gesneriaceae), Petrocosmea Oliv. (Gesneriaceae), and Rhododendron L. (Ericaceae) provide other examples for this trend. These genera have many endemic species in South China but do not have a single one in Hainan (Wang et al., 1998; Fang et al., 2005).

Conservation Status

Only 128 of the endemic seed plants (33%) have been red-listed by the IUCN (IUCN, 2009), or by the China Species Information Service (CSIS, 2009), or by the recent China Species Red List (Wang & Xie, 2004). Eight of these species were previously included in the China Plant Red Data Book (Fu & Jin, 1992) using criteria established by the IUCN in the 1980s. In addition, 27 of the endemics are officially regarded as National Protected Key Wild Plants (First Batch) or Endangered or Rare Species of Chinese Angiosperms by the Chinese Government (Compilation Group of China’s Biodiversity, 1998;Yu,1999). In addition, the conservation status of nine of the most recently described Hainan endemics was assessed using IUCN criteria at the time of publication (Fan et al., 2007; Meng et al., 2007; Yu et al., 2007; Wang, 2008; Liu et al., 2009; He et al., 2009a, b; Zhang et al., 2009). In total, 144 of the seed plants endemic to Hainan have been assigned a conservation status, either by using the IUCN criteria or by being included in governmental protection lists (Table 6). Only one species is regarded as extinct (Lepisanthes unilocularis Leenh. (Sapindaceae); IUCN, 2009) and 85 species have been recognized as critically endangered or endangered. At least 21% of the endemic flora is therefore in urgent need of conservation (Table 6 and 7). The four protected areas included in our study harbor 271 endemic species, representing approximately 68% of the total endemic flora (Table 8). These reserves provide protection for the unique rainforest of Hainan (Fig. 1). Situated in the south of Hainan, Diaoluoshan has the highest number of endemic species (163 spp.). It is estimated that this reserve contains approximately 41% of all the species endemic to Hainan.

Table 6 Conservation Status for Seed Plant Species Endemic to Hainan Island

Number of species with conservation status (percentage of endemic species)a 144 (36) Number of extinct species (percentage of endemic species)b 1 (0.25) Number of critically endangered species (percentage of endemic species)b 40 (10) Number of endangered species (percentage of endemic species)b 45 (11) Number of vulnerable species (percentage of endemic species)b 45 (11) a Data based on original species description, and reports by Fu and Jin (1992), Compilation Group of China’s Biodiversity (1998), Yu (1999), Wang and Xie (2004), CSIS (2009) and IUCN (2009) b Data based on original species descriptions and reports by CSIS (2009) 368 J. Francisco-Ortega et al.

Table 7 Endemic Species Occurring in Four Nature Reserves

Reserve Number of endemic Surface (km2) Vegetation Notes species (percentage of endemic species)a

Bawangling 126 (32) 300 Tropical rainforest Established in 1980 to protect the Hainan Gibbon Diaoluoshan 163 (41) 380 Tropical rainforest Established in 1994 Jianfengling 157 (40) 470 Tropical rainforest Established in 1960. Oldest reserve on Hainan Yinggeling 107 (27) 250 Tropical rainforest Established in 2003. Largest primary rainforest of Hainan Totalb 271 (68) 1,400 (3.5%)c a Including endemic species found outside reserve boundaries b Total refers to endemic species occurring in at least one of the four nature reserves c Percentage refers to total area of Hainan Island

Molecular Phylogenetic Perspective

Molecular phylogenetic data are available for 24 of Hainan’s endemic species. This represents only 6% of the total endemic flora (Table 8). Most of these studies aim to elucidate phylogenetic relationships within or between particular genera, and none have the Hainan endemics as their main research focus. Therefore, any implications from these studies regarding the evolutionary history of the Hainan flora need to be interpreted with caution. None of these previous studies targeted putative relatives of the Hainan taxa and therefore it is not certain to what extent they identify the closest mainland relatives of the endemics. However, there are some patterns that provide insights for the origin and evolution of the Hainan endemics. These DNA phylogenies are published in 23 studies, but only seven of them are based on multiple unlinked DNA regions. Nine of the clades that include Hainan endemics are poorly supported (bootstrap value <74%) and, with the exception of the bamboo genus Bonia, none of the studies include more than 50% of the species of the genera with endemic species. However, Alpinia, Arisaema, Machilus, Michelia, Olea, and Symplocos have been widely sampled, with between 19 species (Olea) and 90 species (Symplocos) having been included. The available phylogenies show that the closest relatives of the Hainan endemics are found in mainland Asia. Mast et al. (2008) indicate that the closest relatives of the Hainan species Heliciopsis lobalata are found in Australia and New Caledonia; however, this phylogenetic study does not include any additional taxa of Heliciopsis. The vast majority of the phylogenies place the Hainan endemics as terminal branches suggesting a recent origin for these taxa. The only exceptions to this are: Olea neriifolia, which is sister to the rest of the subgenus Tetrapilus (Besnard et al., 2009); Alpinia coriacea, which is sister to a clade of eight species within Clade IV of the genus (Kress et al., 2005); and Lingnania hainanensis, which represents the earliest branch in the clade that contains this genus (Sun et al., 2005). The molecular study by Hong et al. (2001) suggests a sister relationship between two Hainan edpatedms nHia sad369 Island Hainan on endemism plant Seed Table 8 Endemic Species Included in Molecular Systematic Studies

Species Samplinga Sister taxon/clade Distribution of sister taxon/clade Reference

Actinodaphne paotingensis Y. C. Yang 13/100 13/100 A. lecomtei C. K. Allen China (Guangdong, Guizhou, Sichuan) Li et al., 2006b, c, d & P. H. Huang Alpinia coriacea T. L. Wu & S. J. Chen 72/230 Clade with eight species of Alpinia Vietnam, Laos, the Philippines, China Kress et al., 2005 Ampelocalamus actinotrichus (Merr. & Chun) 3/13 Polytomy with two additional species India, SE Asia, Nepal, China (Guishou, Yunnan) Guo et al., 2002b S.L.Chen,T.H.Wen&G.Y.Sheng (A.patellaris (Gamble) Stapleton and A. scandens Hsueh & W. D. Li) Arcangelisia gusanlung H. S. Lo 1/4 Anamirta cocculus (L.) Wight & Arn. India, SE Asia, Papua New Guinea, the Philippines Wang et al., 2007bb Arisaema hainanense H. Li, Y. Shiao 77/150 A. rhizomatum C. E. C. Fisch. From India to Vietnam and China Renner et al., 2004b & S. L. Tseng Bambusa malingensis McClure 6/100 Polytomy with two additional lineages (two China (Fujian, Guangxi Guangdong, Hainan, Sungkaew et al., 2009b species of Bambusa and one species of Guangdong, Hainan, Yunnan) Neosinocalamus) Bonia levigata (L. C. Chia, H. L. Fung 3/5 B. saxatiles (L. C. Chia, H. L. Fung, & Y. L. China (Guangdong, Guangxi) Yang et al., 2008 & Y. L. Yang) N. H. Xia Yang) N. H. Xia Chirita heterotricha Merr. 15/140 C. pteropoda W. T. Wang China (extinct in the wild, probably from Guangxi) Li & Wang, 2007 Dehaasia hainanensis Kosterm. 1/35 Alseodaphne hainanensis Merr Hainan, Vietnam Chen et al., 2009b,c Heliciopsis lobata (Merr.) Sleumer 1/10 Polytomy with Virotia neurophylla P. H. Australia, New Caledonia Mast et al., 2008b Weston & A. R. Mast, V. leptophylla (Guillaumin) L. A. S. Johnson & B. G. Briggs, and Athertonia diversifolia (C. T. White) L. A. S. Johnson Lingnania hainanensis (L. C. Chia 5/14 Clade with four species of Bambusa, two India, SE Asia, widespread in China Sun et al., 2005b & H. L. Fung) T. P. Yi species of Dendrocalamus, and four species of Lingnania Lirianthe albosericea Chun & C. H. Tsoong) 2/12 Lirianthe henryi (Dunn) N. H. Xia & C. Y. Wu SE Asia, China (Yunnan) Shi et al., 2000b N. H. Xia & C. Y. Wu 5/12 Polytomy with six additional species of Lirianthe Vietnam, SE Asia, Nepal, widespread in China Kim et al., 2001b, c Machilus monticola S. K. Lee 23/100 Polytomy with six additional Widespread in SE Asia, India, Nepal, Korea, and Japan China Chen et al., 2009b China, lineages (21 species of Machilus) (Guangxi, Guizhou) Table 8 (continued)

Species Samplinga Sister taxon/clade Distribution of sister taxon/clade Reference 7 .FacsoOtg tal. et Francisco-Ortega J. 370 Machilus pomifera (Kosterin.) S. K. Lee 23/100 M. salicoides S. K. Lee China (Guangxi, Guizhou) Chen et al., 2009b Madhuca hainanensis Chun & F. C. How 3/100 Polytomy with 11 additional Widespread Smedmark et al., 2006 worldwide lineages Michelia shiluensis Chun & Y. F. Wu 20/70 Michelia odora (Chun) Nooteboom & B. L. Vietnam, China (Fujian, Guangdong, Guangxi, Kim et al., 2001b, c Chen Hainan, Hunan, Jiangxi, Yunnan) Olea neriifolia H. L. Li 19/40 Clade with six species of Olea SE Asia, the Philippines, Indonesia, China Besnard et al., 2009b (Guangdong, Guangxi, Guizhou, Hainan, Sichuan, Yunnan Phyllanthus hainanensis Merr. 18/800 P. ruber (Lour.) Spreng. Vietnam, Hainan Lee et al., 2006b Polyspora hainanensis (Hung T. Chang) B. 6/40 Polytomy with five additional species of SE Asia, widespread in China Prince & Parks, 2001b M. Barthol. & T. L. Ming Polyspora 5/40 P. chrysandra (Cowan) B. M. Barthol. & T. L. SE Asia, China (Guizhou, Sichuan, Yunnan) Yang et al., 2004b, c Ming Stemona parviflora 4/27 Polytomy with three additional species of Widespread from India to SE Asia, the Philippines, Jiang et al., 2006bb Stemona China, and Japan Stephania hainanensis H. S. Lo & 9/60 S. succifera Hainan Hong et al., 2001b, c Y. Tsoong Stephania succifera H. S. Lo & 9/60 S. hainanensis Hainan Hong et al., 2001b, c Y. Tsoong 3/60 S. brachyandra Diels SE Asia, China (Yunnan) Wang et al., 2007b Symplocos euryoides Hand.-Mazz. 90/250 S. adenophylla G. Don SE Asia, China (Fujian, Guangdong, Guangxi, Wang et al., 2004c, d 74/250 S. adenophylla Hainan, Hunan, Yunnan), the Philippines Fritsch et al., 2006c Symplocos ovatilobata Noot. 90/250 S. viridissima Brand India, SE Asia, China Guangdong, Guangxi, Wang et al., 2004 74/250 S. viridissima Guizhou, Hainan, Xizang, Yunnan Fritsch et al., 2006 Total number of endemic species 24 (6) (percentage of endemic flora) a Number of species included in phylogeny/total number of species in genus b Results based on only one independent DNA marker c Bootstrap support for relevant nodes <74% d Bootstrap support for relevant nodes <74% but Bayesian inference posterior clade probability >80% Seed plant endemism on Hainan Island 371 endemics, Stephania hainanensis and S. succifera, but the clade is weakly supported by a very low bootstrap value of 51%.

Concluding Remarks and Future Research Directions

Hainan has a low level of endemism when compared with other island systems, and its endemic flora represents only a small proportion of the endemic plants of China. Still, however, Hainan has the best preserved tropical forests in China and is the most relevant insular component of the Indo Burma Biodiversity Hotspot. In addition, our study shows that at least 20% of the taxonomic diversity in nine genera is represented only by Hainan endemics, and that 38 genera do not have any additional endemic species in the rest of China. Our review did not cover the rest of the native flora of Hainan, but we anticipate that because of the geographical location of Hainan, a large proportion of the genera occurring in Hainan are present only in Vietnam or the rest of SE Asia and do not reach mainland China or Taiwan (as suggested by Zhu & Roos, 2004). Clearly the endemic flora of Hainan is an important component of the natural heritage of China and a priority for conservation. Nevertheless, our study shows that there are still major unknowns concerning the biology, ecology, and phylogenetics of these endemic species. Based on this study we argue that future research/conservation actions for the endemic flora of Hainan should focus on developing: (1) a red list that includes all 397 endemic species, (2) exhaustive floristic studies of the protected areas that involve additional plant exploration, (3) molecular phylogenetic and population genetic studies with a primary focus on the endemics, (4) comprehensive studies to understand the ecological interactions and their importance in the biology of the endemic species, and (5) eco- geographical studies to identify hot spots of endemism within Hainan.

Acknowledgements We dedicate this paper to Dr. Jose María Durán-Altisent from Escuela Técnica Superior de Ingenieros Agrónomos de Madrid (Spain). His human and academic values as undergraduate mentor (1984–1986) have marked the professional trajectory of JFO. We are grateful to J.-S. Lei, K.-J. Zhang, and Q.-S. Yan for their help and guidance with our review on the geology of Hainan. Nicholas J. Turland shared with us unpublished data concerning the number of endemics from China. This is contribution 180 from the Tropical Biology Program of Florida International University. The Nanjing University (NU) 985 II program supported a research visit by HL and JFO. to the School of Life Science of NU during the summer of 2008. Summer research funds (2008–2009) from Fairchild Tropical Garden supported the studies of HL and JFO in China.

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