Features and distribution patterns of Chinese endemic seed plant species

Transcription

1 Journal of Systematics and Evolution 49 (2): (2011) doi: /j x Research Article Features and distribution patterns of Chinese endemic seed plant species 1,2,3 Ji-Hong HUANG 1,4 Jian-Hua CHEN 5 Jun-Sheng YING 1 Ke-Ping MA 1 (State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing , China) 2 (Graduate University of Chinese Academy of Sciences, Beijing , China) 3 (Center for Documentation and Information, Institute of Botany, Chinese Academy of Sciences, Beijing , China) 4 (Zhejiang Normal University, Jinhua , China) 5 (Research Center of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing , China) Abstract We compiled and identified a list of Chinese endemic seed plant species based on a large number of published references and expert reviews. The characters of these seed plant species and their distribution patterns were described at length. China is rich in endemic seed plants, with a total of species (accounting for 52.1% of its total seed plant species) belonging to 1584 genera and 191 families. Temperate families and genera have a significantly higher proportion of endemism than cosmopolitan and tropical ones. The most primitive and derived groups have significantly higher endemism than the other groups. The endemism of tree, shrub, and liana or vine is higher than that of total species; in contrast, the endemism of herb is lower than that of total species. Geographically, these Chinese endemic plants are mainly distributed in Yunnan and Sichuan provinces, southwest China. Species richness and proportion of these endemic plants decrease with increased latitude and have a unimodal response to altitude. The peak value of proportion of endemism is at higher altitudes than that of total species and endemic species richness. The proportions of endemic shrub, liana or vine, and herb increase with altitude and have a clear unimodal curve. In contrast, the proportion of tree increases with altitude, with a sudden increase at 4000 m and has a completely different model. To date, our study provides the most comprehensive list of Chinese endemic seed plant species and their basic composition and distribution features. Key words biodiversity, conservation, distribution pattern, endemism, flora of China, seed plants. Endemism is one of the core issues in biogeography (Cain, 1944; Takhtajan, 1986; Crisp et al., 2001; Lomolino et al., 2006), and an essential component of any study that investigates the characters, origins, and evolution of flora and fauna (Good, 1974; Cox & Moore, 2005; Lomolino et al., 2006). The study of endemic plant distribution plays an important role in understanding the phylogenetic history of flora because the distribution of a species is closely related to its evolutionary history (Richardson, 1978; Wu, 1980; Ying, 1996; McGlone et al., 2001; Wood, 2006; Burke, 2007). The study on distribution patterns of endemic species is of great importance in biodiversity conservation. In recent decades, increasingly intensive human activities have led to the rapid destruction and fragmentation of natural habitats and a corresponding decrease in worldwide biodiversity (Pimm et al., 1995; Balmford et al., 2003; Jenkins et al., 2003). Therefore, effectively protecting biodiversity resources has become one of the core concerns (Pimm et al., 1995; Reid, 1998). A large Received: 14 November 2010 Accepted: 7 January 2011 Author for correspondence. kpma@ibcas.ac.cn; Tel.: ; Fax: number of methods and standards have been widely used to study biodiversity and conservation (Wilson & Francis, 1988; Heywood & Watson, 1995; Pimm et al., 1995; Olson & Dinerstein, 1998; Gaston, 2000; Myers et al., 2000; Myers, 2003; Brummitt & Lughadha, 2003; Zhang & Chen, 2003; Brooks et al., 2006). The identification of biological hotspots is an increasingly popular approach in biodiversity conservation (Mittermeier et al., 1998; Olson & Dinerstein, 1998; Myers et al., 2000; Myers, 2003; Brummitt & Lughadha, 2003; Brooks et al., 2006). Endemism has become an increasingly common and irreplaceable surrogate for identifying the world s biodiversity hotspots (Myers et al., 2000; Mittermeier et al., 2005; Orme et al., 2005; Lamoreux et al., 2006). On one hand, endemic species are potentially threatened because they distribute only in restricted areas (Linder, 1995; Gaston & Blackburn, 1996). On the other hand, humans have no capabilities for protecting all species due to their limited available resources (Myers et al., 2000). China spans a broad geographical area (9.6 million km 2 and a span of more than 50 latitude), with enormous variations in geographical and topographical features, from mostly plateaus and mountains in the west

2 82 Journal of Systematics and Evolution Vol. 49 No to lower lands in the east. These varying land features have resulted from the dissection and elevation of mountains created by the collision of the Indian subcontinent with the Asian continent approximately 50 million years ago (Editorial Committee of China s Physical Geography, 1985). Thus, its topography is described typically as the Three Steps : the First Step includes mainly the highest mountains (over 3500 m), for example, the Himalayas, where the highest point on earth, Mount Everest, can be found; the Second Step consists primarily of mid-mountains ( m); and the Third Step is comprised of lower mountains ( m) and plains (Editorial Committee of China s Physical Geography, 1985). Complex topographies, special land and sea locations, and its ancient geological history have resulted in the complicated and diverse climate of China (Editorial Committee of China s Physical Geography, 1985) and provide abundant habitats for plants and animals (Wu & Wang, 1983; Ying, 2001). Hence, China supports vegetational continuity from tropical, subtropical, and temperate to boreal forests (Axelrod et al., 1996), thus contributing to a major center of survival, speciation, and evolution for vascular plants in the world (Axelrod et al., 1996; Qian, 2002). China is one of the world s mega-biodiversity countries, and one of the richest countries in terms of plant biodiversity (Wu & Wang, 1983; McNeely et al., 1990; Fu et al., 1993; Mittermeier et al., 1997). The total number of vascular plant species in China is more than (Compilation Group of Study of China s Biodiversity, 1998; Editorial Committee of Flora Reipublicae Popularis Sinicae, 2004). In addition, its seed plant species diversity ranks third in the world, next to Brazil and Colombia (McNeely et al., 1990; Liu et al., 2003). Flora in China is highly endemic (Wu & Wang, 1983; Fu et al., 1993; Zuo & Fu, 2003). Compared to its neighboring countries of equal latitude and longitude, China has very high levels of plant endemism (Ying, 2001; Zuo & Fu, 2003). However, China is one of the countries with the highest number of threatened species in the world (Jenkins et al., 2003). Of the World Wildlife Fund s Global 200 most Critical and Endangered Ecoregions, 17 are located in or intersected with China (Olson & Dinerstein, 2002). Furthermore, of the 34 global biodiversity hotspots identified by Conservation International (Mittermeier et al., 2005), four either intersect with or are located in China. Thus, diverse ecosystems in China play an important role in conserving global biodiversity. Despite the conservation priority of these internationally recognized hotspots, human activities continue to threaten the natural areas in China. China is suffering from accelerated land degradation; wetlands are shrinking rapidly; pasturelands are severely overgrazed, and invasive species are becoming increasingly problematic (Liu et al., 2003; Cyranoski, 2008). The International Union for Conservation of Nature (IUCN) 2008 Red List places China among the countries with the most threatened birds, mammals, conifers, and cycads (Vié et al., 2009). In Asia, China takes first place among countries with the most threatened species, including mammals, birds, reptiles, amphibians, fishes, and plants (Vié et al., 2009). Although many studies on endemism of Chinese flora have been carried out, data are still not enough to provide systematic guidance for biodiversity conservation in China, especially at species level. At generic level, there are a number of publications that provide relevant information. China has four endemic families (Wu & Wang, 1983; Wang, 1992), 243 endemic genera (Ying & Zhang, 1994) and three centers of endemism in terms of endemic genera (Ying & Zhang, 1994). At species level, the information that has been gathered on biodiversity is more limited. There are many published reports relevant to Chinese endemic species, but most research has focused only on small or local scales, such as provinces, floristic regions (mostly relevant to the province), lakes, islands, or mountain tops (Xing et al., 1995; Peng, 1997; Qi et al., 1998; Fu, 1999; Yu & Xiao, 1999; Zhang & Zhao, 2000; Li et al., 2001; Feng & Pan, 2004). Other studies have focused on a group, such as a specific family or genus (Ying & Li, 1981; Li et al., 2009). These investigations may have played an important role in conserving local or regional plant diversity and individual taxa. However, they cannot provide substantial scientific reference to decision-making bodies regarding biodiversity conservation for the whole country. In this study, we identify a list of Chinese endemic seed plant species and determine their distribution patterns to provide scientific data for Chinese biodiversity conservation. 1 Material and methods 1.1 Concepts and terminology Endemism itself is a scale-dependent and relative concept; thus, the definition of endemic taxa depends on the study area (Cain, 1944; Good, 1974; Anderson, 1994; Crisp et al., 2001). In this paper, we use the term Chinese endemic taxa to refer to the taxa that occur naturally in China and nowhere else in the world, and are completely based on administrative boundaries. Similarly, the term local endemic species indicates

3 HUANG et al.: Chinese endemic seed plant species 83 species that are found in any single province. In addition, we also use the term endemic genus to refer to genera that are confined entirely to China. Based on the definite number of endemic species and the total number of species for each family and genus, we use two terms to reflect the endemism of higher taxa: one is generic endemism, which is the ratio of number of endemic species to total number of species within each genus; the other is familial endemism, which is the proportion of endemic species from all species within each family. China is comprised of 23 provinces, five autonomous regions and four municipalities. In this study, four municipalities are merged into their original provinces, not only because they have small areas, but also because some of them have been separated recently from their corresponding province; both municipalities and their corresponding provinces are described as the whole administrative unit in many studies. In addition, a province is equal to an autonomous region in terms of administrative level; thus, we consider all provinces and autonomous regions as a province for the convenience of discussion. 1.2 Data sources and dataset Main data sources were publications, such as floras, monographs, and articles. A master database for Chinese seed plants was created. The database was initially based on Flora Reipublicae Popularis Sinicae (Editorial Committee of Flora Reipublicae Popularis Sinicae, ) and Flora of China (Wu et al., ). The former is a comprehensive list of Chinese seed plants published completely, whereas the latter is the English revision of the former, which has published 11 volumes as of To update and complete the list of Chinese seed plants and their related information, we also referred to other important works describing the distribution of Chinese plants, including the Higher Plants of China (Editorial Committee of Higher Plants of China, ), two Compilations of Type Specimen from China (Jin, 1994, 1999), and more than 150 volumes of floristic books related to provincial and regional flora, as well as articles published before We have listed all references in Supplementary Material 1. Based on the above sources, we compiled a database of seed plant species native to China using Microsoft Access (Prague & Irwin, 1999). The database consisted of species names, family names, life forms, altitudes, distributions at the provincial level, and endemic status of each species. Distribution information for the presence/absence and endemic/nonendemic status of each seed plant species was documented for each province. Alternatively, the latitude locations of species were taken as the latitude of the centroids of relevant provinces, which were extracted from the Chinese administrative map ( using ArcGIS 9.0 (ESRI, 2004). Other information on the number of species and the floristic elements for each family and genus was based on a published monograph (Wu et al., 2006). 1.3 Identification of endemic species Recording all Chinese seed plant species relies on a large quantity of published reviews and expert opinion. In this manner, we completed an inventory of all seed plants of Chinese flora. The inventory included indigenous species only; that is, we excluded all naturalized, exotic, and cultivated species. From our inventory of all seed plants of Chinese flora, we selected all seed plants distributed only in China based on the publications we consulted. Furthermore, we sought the expert opinion of 55 Chinese taxonomists to review the selected inventory. We required all experts to conform to the following three conditions for the selected list: (i) exclude species distributed outside China; (ii) complement species omitted in our selected list; and (iii) provide all publications and relevant information supporting their conclusions. These conditions were required so that we could complement and revise our list as accurately and verifiably as possible. Ultimately, we obtained a list of Chinese endemic species of seed plants (Supplementary Material 2). 1.4 Statistics, analysis, and mapping We analyzed the compositions of both the Chinese endemic species identified in this study and their higher taxa (family and genus), and counted the quantitative characteristics of each main group in terms of different life forms. Each species was placed in a genus, a family, and an order. The placement of species in genera and families followed the phylogenetic tree of Zheng & Fu (1978) for gymnosperms and that of Engler (Schulze- Menz, 1964) for angiosperms, whereas the designations of orders followed that of APGII (APG, 2003) for angiosperms. Orders of seed plants were divided into six groups: gymnosperms, basal angiosperms, monocots, basal eudicots, rosids, and asterids. ANOVA and Tukey s multiple comparisons (Bretz et al., 2010) were carried out to assess endemism differences in floristic elements and taxonomic groups. To detect the distribution pattern of Chinese endemic species in the entire country, we took the province as the operational geographical unit (OGU) and calculated four indices separately: Chinese endemic

4 84 Journal of Systematics and Evolution Vol. 49 No seed plants species richness; local (provincial) endemic seed plant species; weighted endemism (Williams & Humphries, 1994; Crisp et al., 2001); and proportion of endemism (i.e., the ratio of Chinese endemic species to total species native to China). We used Equation (1) to calculate the weighted endemism. In Equation (1), n is the number of species in the focal province, and W i is the weight of species i, which is the inverse of its range (the range equates to the number of provinces in which species i occurs): WE = n W i (1) i=1 We used Pearson s correlations to test the correlations of any pair of indices using R software (Everitt & Hothorn, 2006) and generated output maps of four indices with five levels for each index using Jenks optimization method (Jenks, 1967) using ArcGIS. We also analyzed patterns of endemic species richness and proportion of endemism of four life forms along latitudinal gradients. Given that the relationship of the number of taxa and the land area is usually exponential (He et al., 1996), we used an area-adjusted species density equation (Tang et al., 2006) as a measure of diversity (Qian, 1998) to minimize the effect of area size on the relationship of species richness and latitude. This equation is given in Equation (2), where D is the species density for a province, S is the number of species for the province, and A is the area of the province. We also used Pearson s correlations to test the correlations of endemic species richness and proportions of endemism. Linear model (Legendre & Legendre, 1998) was applied to check the relationship of endemic species richness and proportion of endemism with latitudinal gradients. D = S/ log(a) (2) We obtained data on native species based on altitude. To detect the distribution patterns of Chinese endemic species and proportions of endemism from different life forms along an altitudinal gradient, we divided the altitude into 58 equal bands from 0 to 5800 m and obtained the number of species in each 100 m band as the species richness within the band using R software (Everitt & Hothorn, 2006), and computed for total species richness, Chinese endemic species richness, non-endemic species richness, and proportion of total endemics as well as proportions of endemics from different life forms for each altitudinal band. Table 1 Number of endemic species of seed plants in China and their proportion Group NCES NCET NTS NTT PES PET Tree Shrub Liana & vine Herb Total NCES, number of endemic seed plant species; NCET, number of endemic seed plant taxa (include species, subspecies, and varieties); NTS, number of total seed plant species; NTT, number of total seed plant taxa (include species, subspecies, and varieties); PES, percentage of endemic seed plants species in each group (%); PET, percentage of endemic seed plants taxa in each group (%). 2 Results 2.1 Composition analysis Based on our data, China has seed plant species, of which are endemic seed plant species (excluding infraspecific taxa), accounting for 52.1% of the total species of seed plants in China (Table 1). The total number of all taxa, including infraspecific taxa, is provided in Table 1. Among the four groups, in terms of life forms, shrubs have the highest proportion of endemic species, followed by trees, lianas or vines, and then herbs. In terms of the total number of endemic species, herbs have the highest number, followed by shrubs, trees, and then lianas or vines (Table 1). The endemic species identified in this study belong to 1584 genera among which, monotypic, oligotypic, and multitypic genera (Wu & Wang, 1983) contain 134, 331, and 1119 genera, respectively. There are 203 endemic genera, which consist of 134 monotypic genera, 54 oligotypic genera, and 15 multitypic genera, with 476 endemic species. Monotypic and oligotypic genera account for 92.6% of the endemic genera, whereas multitypic genera account for 7.4% only; these endemic genera belong to 68 families. According to the number of endemic genera, Gesneriaceae, Asteraceae, Poaceae, and Lamiaceae are the largest families; the numbers of endemic genera belonging to these families are 29, 18, 13, and 10, respectively. Phylogenetically, these endemic genera contain various groups from the primitive to derived (Wu & Wang, 1983; Axelrod et al., 1996). Moreover, a large number of relic groups are included in the primitive groups (Wang, 1992; Axelrod et al., 1996). Most species that belong to endemic genera are rare, threatened, or endangered (Fu et al., 1993; Wang & Xie, 2004) and have also been listed as nationally protected plants in China, such as ginkgo (Ginkgo biloba Linnaeus), silver fir (Cathaya argyrophylla Chun & Kuang), metasequoia (Metasequoia glyptostroboides Hu & W. C. Cheng), Taiwan fir (Taiwania cryptomerioides Hayata), golden larch (Dipteronia

5 HUANG et al.: Chinese endemic seed plant species 85 Table 2 Top 20 Chinese seed plant genera, in terms of number of endemic species No. Genus NCES PEG 1 Rhododendron (Ericaceae) Pedicularis (Scrophulariaceae) Carex (Cyperaceae) Primula (Primulaceae) Corydalis (Papaveraceae) Berberis (Berberidaceae) Salix (Salicaceae) Impatiens (Balsaminaceae) Saussurea (Asteraceae) Aconitum (Ranunculaceae) Saxifraga (Saxifragaceae) Ilex (Aquifoliaceae) Gentiana (Gentianaceae) Astragalus (Fabaceae) Rubus (Rosaceae) Begonia (Begoniaceae) Acer (Aceraceae) Delphinium (Ranunculaceae) Elatostema (Urticaceae) Lysimachia (Primulaceae) NCES, number of endemic seed plants species; PEG, percentage of endemic species in a genus in China. Table 3 Top 20 Chinese seed plant families, in terms of number of endemic species No. Family NCES PEF 1 Compositae Gramineae Leguminosae Ranunculaceae Rosaceae Ericaceae Orchidaceae Labiatae Scrophulariaceae Liliaceae Gesneriaceae Primulaceae Saxifragaceae Rubiaceae Umbelliferae Lauraceae Cyperaceae Berberidaceae Gentianaceae Theaceae NCES, number of endemic seed plants species; PEF, percentage of endemic species in a family in China. sinensis Oliver), eucommia bark (Eucommia ulmoides Oliver), and Chinese dove tree (Davidia involucrata Baillon) (Wang, 1992; Fu et al., 1993; Wang & Zhang, 1994). Among the top 20 genera in terms of the number of endemic species, the endemics from these genera are the dominant species, and they exceed half of the native species in China, with the exception of Carex and Astragalus (Table 2). Moreover, herbs are the dominant groups in these top genera. The endemic species identified in this study belong to 191 families, among which 39 contain more than 100 endemic species, such as Compositae, Gramineae, Fabaceae, Ranunculaceae, and Rosaceae. A total of endemic species belong to these 39 families, which account for 80.5% of the all the endemic species in China. Seventy-four families, such as Oleaceae, Celastraceae, Verbenaceae, and Campanulaceae, include endemic species each, for a total of 2669 species, which account for 17.9% of the endemic species. Among the top 20 families in terms of number of endemic species, herbs are also the dominant groups. Berberidaceae, Gesneriaceae, Theaceae, Primulaceae, and Lauraceae have the highest proportion of endemism (Table 3). Some families with more than 100 endemic species also have high percentages of endemism, such as Begoniaceae (134 endemic species, 87.0%), Balsaminaceae (188 endemic species, 81.4%), Aceraceae (127 endemic species, 79.4%), and Aquifoliaceae (141 endemic species, 74.4%), although they are not included in these top families. Based on all three floristic elements, the temperate families and genera have a significantly higher proportion of endemism than cosmopolitan and tropical families (P < 0.001) and there is no significant difference in cosmopolitan and tropical families and genera (Fig. 1). The proportion of endemism with respect to phylogenetic groups is distributed unevenly. At family level, the most primitive group, gymnosperms, and most derived group, asteroids, have significantly higher (P < 0.001) proportions of endemism than the other groups (Fig. 2: A). At genus level, the proportions of endemism in phylogenetic groups have the same pattern as those at family level (Fig. 2): the most primitive and derived groups have higher proportions of endemism than the other groups (Fig. 2: B). 2.2 Geographical distribution patterns Endemism of Chinese flora has an uneven distribution pattern. Chinese endemic species richness, local endemic species richness, weighted endemism, and proportion of endemism are the highest in southwest China. The lowest values can be found in northeast China, except in Heilongjiang and Jilin provinces, which are next to Ningxia Hui Autonomous Region in local endemic species (Table 4 and Fig. 3). The distribution patterns of Chinese endemic seed plant species are highly congruent with the total seed plant species when using province as the OGU (r = 0.954, P < 0.001). Chinese endemic species richness is concentrated in southwest China, such as Yunnan and Sichuan provinces, with 8577 Chinese endemic

6 86 Journal of Systematics and Evolution Vol. 49 No Fig. 1. Proportion of endemism based on the proportion of Chinese endemic species in all native species in the world for each family (A), genus (B), and three major types of geographical distributions (i.e., cosmopolitan, temperate, and tropical). Letters a and b show the results of multiple comparisons. The same letters indicate that there is not a significant difference between two groups; conversely, different letters indicate that there is a significant difference between groups. species, which account for 57.4% of all the Chinese endemic species. Among Chinese endemic seed plants, 8307 species, which account for 55.6% of Chinese endemic seed plants, are local endemic species at the provincial level. Yunnan Province is the distribution center of local endemic species richness with 2585 species, which account for 31% of all the total local endemic species. The OGU with the second highest local endemic species richness is Sichuan Province with 1393 local endemic species. Local endemic seed plant species richness in the other provinces has the same pattern as Chinese endemic seed plant species (r = 0.903, P < 0.001): the farther from the distribution center, the lower the species number. The category map of local endemic species is a little different from the map of Chinese endemic species (Fig. 3: A, B). Nine provinces have been downgraded by one level, including Sichuan, Guizhou, Hunan, Hubei, Shaanxi, Gansu, Jiangxi, Anhui, and Henan. In comparison, two provinces have been upgraded by two levels, including Xinjiang and Taiwan, and Hainan Province has been upgraded by one level. Among the 28 OGUs, Ningxia Province has the lowest local endemic species richness, with only nine species. The weighted endemism of Chinese endemic species is inversely proportional to their range (number of provinces). A map that resembles the pattern of Chinese endemic species richness was produced (Fig. 3: C) (r = 0.967, P < 0.001). A slightly different pattern shows that all provinces can change no more than one category. The patterns of proportion of endemism are different from that of the other indices (Fig. 3). Sichuan Province, rather than Yunnan Province, has the highest endemism ratio as a distribution center. In addition, the proportion of local endemic species in Taiwan is higher than that in Hainan Province. 2.3 Latitudinal and altitudinal distribution patterns Chinese endemic seed plant species richness increases with decreasing latitude. Chinese endemic species richness is negatively correlated to latitude (r = , P < 0.001, Fig. 4), which indicates that

7 HUANG et al.: Chinese endemic seed plant species 87 Fig. 2. Proportion of endemism based on the proportion of Chinese endemic species in all native species in the world for each family (A), genus (B), and six major phylogenetic groups: A, gymnosperms; B, basal angiosperms; C, monocots; D, basal eudicots; E, rosids; F, asterids. endemic species richness increase along a latitudinal gradient from north to south. The correlation between total species richness and Chinese endemic species richness is significantly high (r = 0.954, P < 0.001). Results for different groups with respect to life form show that the proportion of endemism decreases significantly with the increase in latitude (Table 5). The proportions of endemism from tree, shrub, and liana or vine are higher than that of total species; only the proportion of endemism of herbs is lower than that of total species. From linear models of the four life forms for latitudinal gradients, the rank of the slope is liana, followed by shrub, tree, and then herb (Fig. 5). Total species richness, Chinese endemic species richness, and proportion of endemism have a clear, unimodal response curve along altitudinal gradients (Fig. 6). Total species richness has a monotonic and steeply increasing trend from 0 to 800 m, whereas it has a clear and gentle increasing trend from 800 to 1400 m; from 1400 to 2000 m, this pattern decreases slightly, but higher than 2000 m, species richness decreases sharply up to 5800 m. Total species richness and endemic species richness have significantly identical patterns along altitudinal gradients (r = 0.965, P < 0.001). The proportion of endemism differs from total species richness and endemic species richness along altitudinal gradients. The proportion of endemism peaks at a slightly higher level than total species richness but lower than endemic species richness (Fig. 6). The distribution patterns of the proportion of endemism with increased altitude for shrub, liana or vine, and herb have a clear unimodal curve similar to that of total species richness. In contrast, the distribution pattern of the proportion of endemism for tree with increased altitude is completely different from that of total species richness: it has a sudden increase at 4000 m (Fig. 7). 3 Discussion and conclusions 3.1 Percentage of endemism Estimations of the percentage of Chinese endemic plants have been reported in a number of publications (WCMC, 1992; Groombridge & Jenkins, 2000; Zuo & Fu, 2003), which range from 50% to 60% (He & Ma, 1997). The percentages differ due to lack of data on Chinese flora. The first complete checklist of seed plants in China was not published until 2004 (Editorial

8 88 Journal of Systematics and Evolution Vol. 49 No Table 4 Value of four indices and rank of each Chinese province Code Province NCES NLES WE PE 1 Heilongjiang Jilin Liaoning Neimenggu Hebei Shanxi Shandong Henan Shaanxi Ningxia Gansu Qinghai Xinjiang Anhui Jiangsu Zhejiang Jiangxi Hunan Hubei Sichuan Guizhou Fujian Taiwan Guangdong Guangxi Yunnan Xizang Hainan NCES, number of endemic seed plants species; NLES, number of local endemic seed plants species; PE, percentage of Chinese endemic species in all Chinese native species; WE, weighted endemism. Committee of Flora Reipublicae Popularis Sinicae, 2004). The total number of seed plants in China is more than species (Editorial Committee of Flora Reipublicae Popularis Sinicae, 2004), third in the world after Brazil and Colombia (McNeely et al., 1990; He & Ma, 1997; Compilation Group of Study of China s Biodiversity, 1998). Our study concludes that endemic seed plants account for 52.1% of the seed plants in China. To our knowledge, in the northern hemisphere, China is the richest country in both total number of seed plants and endemic seed plants, and also the country with the highest percentage of endemism. Endemism favors the most primitive and derived groups. Our study provides the first comparison of the proportion of endemism between life form groups and between phylogenetic groups. The results from this study support that woody plants, including trees and shrubs, have a higher level of proportion of endemism than herbs. Woody plants are generally accepted as more primitive than herbs in view of the evolution of angiosperms because woody plants are dominant in the earliest angiosperm fossils; this proposition suggests that primitive life forms have a higher proportion of endemism of flora in China. As shown in this study, the gymnosperms, basal angiosperms, and asterids have significantly higher proportions of endemism than the other groups, with respect to different phylogenetic groups. These findings show that the most primitive and the most derived groups have higher proportions of endemism, and support a widely held notion that China is an important center of survival and differentiation of plants (Raven & Axelrod, 1974; Axelrod et al., 1996; Qian & Ricklefs, 2004a). 3.2 Potential causes of distribution pattern Many factors can potentially affect species richness, including contemporary environments, geologic histories, biotic histories, and biotic interactions. At the regional scale (large scale), geologic history factors are dominant (Wright et al., 1993; Qian & Ricklefs, 2004b), and affect or control directly or indirectly the speciation, differentiation, migration, and extinction of plants (Takhtajan, 1969; Raven & Axelrod, 1974; Tiffney, 1985; Latham & Ricklefs, 1993; Axelrod et al., 1996). These geologic history factors include the formation and changes in land and sea structures, rapid change of climate, high mountains or large-scale uplifts of the plateau, and the complexity and diversity of regional eco-environment. Generation of endemic species is also directly derived from these four processes. Thus, those factors that influence the geographical distribution patterns of species richness also influence the geographical distribution patterns of endemic species richness. A difference is that geologic history factors may exert more important influence on endemic species richness than species richness (Qian & Ricklefs, 2004b). China has high species richness, primarily because of its complicated geological features and history, land and sea locations, and diverse climates (Wu & Wang, 1983; Axelrod et al., 1996; Ying, 2001; Wu et al., 2007), and partly because it has not suffered during the Neogene period or in later climatic changes (Raven & Axelrod, 1974; Hu, 1980; Latham & Ricklefs, 1993; Qian & Ricklefs, 1999). The distribution patterns of both total species diversity and endemic species diversity in China are similar. The high levels of Chinese endemic plant richness should share the impact of these geologic history factors. Moreover, the southwestern region of China, including Yunnan and Sichuan provinces, which are roughly situated in the Second Step, are bordered on the west by the Qinghai-Tibetan plateau and are located at the meeting point of the tropical monsoon regions of southern Asia and Indo-China, the Tibetan plateau region, and the eastern Asia monsoon region (Wu & Wang, 1983). High topographic heterogeneity, relatively stable and diverse climate types, and a variety of vegetation types have been reported as essential in plant survival, speciation, and differentiation (Linder,

9 HUANG et al.: Chinese endemic seed plant species 2001; McGlone et al., 2001; Qian, 2001; Jansson, 2003; Tribsch, 2004; Casazza et al., 2008). Accordingly, the high level of endemic species richness in both provinces results likely from a combination of complex geological history, topography, climate, and vegetation in China (Wang & Zhang, 1994; Ying & Zhang, 1994; Yang & Zuo, 1998). Based on the comparison of distributions of endemism between mainland China and its islands, including Taiwan and Hainan, geologic history factors contribute significantly to the distribution of endemic plants. Most Chinese endemic species in Taiwan and Hainan are local species endemic to both islands. These findings support a widely held notion that endemic taxa are rich in ancient mainland islands and ocean islands because ancient flora are preserved and developed separately (Wang, 1992). The proportion of local endemic species in Taiwan is higher than that in Hainan, which may be attributed to its earlier separation from the mainland (Wang, 1992; Wu et al., 2006). 89 Taiwan was formed during the Oligocene period (23 34 Myr), whereas Hainan was completely separated from the mainland during the Holocene period (only years ago) (Editorial Committee of China s Physical Geography, 1980). Islands have high levels of endemism (Whittaker & Ferna ndez-palacios, 2007), and harbor higher concentrations of endemic species than continents do (Wang, 1992). The number and proportion of endemic species increase with increasing isolation, island size, and topographic heterogeneity (Wang, 1992; Price, 2004). 3.3 Zonal distribution of endemic plants Chinese endemic seed plants species richness decreases with increasing latitude, which shows a high degree of consistency with the total number of seed plant species throughout China. The fundamental broad-scale pattern concerning species richness is the increase in diversity from polar to equatorial regions (Brown, 1995; Rosenzweig, 1995; Gaston, 1996; Willig et al., 2003). Fig. 3. Distribution of Chinese endemic species diversity by province as an operable geographical unit. A, Chinese endemic species richness. 1, Heilongjiang; 2, Jilin; 3, Liaoning; 4, Neimenggu; 5, Hebei; 6, Shanxi; 7, Shandong; 8, Henan; 9, Shaanxi; 10, Ningxia; 11, Gansu; 12, Qinghai; 13, Xinjiang; 14, Anhui; 15, Jiangsu; 16, Zhejiang; 17, Jiangxi; 18, Hunan; 19, Hubei; 20, Sichuan; 21, Guizhou; 22, Fujian; 23, Taiwan; 24, Guangdong; 25, Guangxi; 26, Yunnan; 27, Xizang; 28, Hainan. B, Local (provincial) endemic species richness. C, Weighted endemism. D, Proportion of endemism. The Chinese administrative map was downloaded from the National Fundamental Geographic Information System in China ( Levels I V represent five levels for each of the above four indices using Jenks optimization method (Jenks, 1967). C 2011 Institute of Botany, Chinese Academy of Sciences

10 90 Journal of Systematics and Evolution Vol. 49 No Fig. 4. Relationship between Chinese endemic species richness and latitude. Chinese endemic species richness indicates the density of Chinese endemic species richness for each province, and is calculated using the equation D = S/ log(a) whered is the species density for a province, S is the number of species for the province, and A is the area of the province. Fig. 5. Relationship between the proportions of endemism and latitude. The proportions of endemism indicate the proportions of Chinese endemic species in groups in terms of life forms (i.e. tree, shrub, liana or vine, and herb). Many different mechanisms have been suggested to generate systematic latitudinal variations in species diversity (Lomolino et al., 2006). These include explanations based on chance, historical perturbation, environmental stability, habitat heterogeneity, productivity, and interspecific interactions (Gaston, 2000). Our results show that, at a large scale, patterns of species diversity changing with latitudinal gradients appear to be consistent with both endemic species and total species. Our study also shows that all proportions of endemism from different life form groups decrease with increasing latitude. This observation indicates that low latitudinal tropical and subtropical regions tend to have a high degree of endemism, which may have resulted from habitat heterogeneity in these regions; habitat heterogeneity is favorable to maintaining previous diversity and creating new species because of an expansion in the number of partitionable niche dimensions (MacArthur & MacArthur, 1961; Cramer & Willig, 2005). Altitudinal distribution patterns show that Chinese endemic plant richness and total species richness are highly consistent along altitudinal gradients. Whether or not total species richness and endemic species richness represent the same property is still controversial (Vetaas & Grytnes, 2002; Zhang et al., 2009). The mechanisms of altitudinal patterns of species diversity have been discussed widely (Stevens, 1992; Kessler, 2000, 2002; Vetaas & Grytnes, 2002). The mid-domain effect (MDE) (Colwell & Hurtt, 1994; Colwell & Lees, 2000) and Rapoport s rule (Stevens, 1989, 1992) are two popular hypotheses that attempt to explain the pattern of species richness along altitudinal gradients. However, they are unable to justify all altitudinal patterns of species richness because altitude is a complex of different factors, not just a single definite one (Shen & Lu, 2009; Wang et al., 2009). Altitudinal patterns of endemic species diversity may have resulted from the combination of several physical, historical, and other factors. Peak value of the proportion of endemism is different from that of Chinese endemic species richness, indicating that the middle altitude region facilitates endemism. This observation may imply that MDE (Colwell & Hurtt, 1994) influences the patterns of proportion of endemism with altitudinal gradients; however, the patterns of proportion of endemism between tree and other life forms are not identical. Obviously, tree groups have a narrower distribution range than the other groups; thus, the unimodel curve is not the unique general altitudinal pattern of proportion of endemism, and may imply that MDE Table 5 Analysis of variance of linear model of relationship of the proportion of endemism and latitude Beta Adjusted R- Group (slope = Beta ) squared F P Tree <0.01 Shrub <0.01 Liana or <0.001 vine Herb <0.05 All < < P 0.05; < P 0.01; P

11 HUANG et al.: Chinese endemic seed plant species 91 Fig. 6. Relationship between total species richness, Chinese endemic species richness, proportion of endemism, and altitude. has a limited effect on the proportion of endemism of restricted groups. 3.4 Essential to global biodiversity conservation More than vascular plant species occur in China. Based on our data, more than 50% of the seed plants in China are endemic, 55% of which are local endemic species especially important for the conservation of biodiversity worldwide, because endemic species which occur only in restricted areas are unique and potentially threatened (Linder, 1995; Gaston & Blackburn, 1996). These endemic species consist of many relic and primitive groups. Substantial fossil evidence and the distribution of extant species indicate that many Chinese endemic genera that were once widely distributed in Laurasia during the Tertiary period (or even earlier) now survive only in China (Ying & Zhang, 1994; Axelrod et al., 1996; Qian & Ricklefs, 1999), such as Ginkgo, Metasequoia, Pseudolarix, Camptotheca, Dipteronia, Davidia, and Eucommia. China is considered not only an important center of refugia, but also an important center of speciation and evolution for vascular plants (Raven & Axelrod, 1974; Ying & Zhang, 1994; Axelrod et al., 1996; Qian, 2002). Moreover, flora of China are thought to be a mixture of Laurasian, Gondwanan, and Tethyan elements (Wu, 1988); thus, many of its relic and endemic taxa can provide unique opportunities for exploring numerous issues concerning global biogeography. Acknowledgements We are particularly grateful to Mr. Jian-Hua HUANG who read the entire paper and gave us constructive suggestions for its improvement. We are also grateful to many experts who helped us identify the ultimate endemic plant list. They are Zi-Yu CAO, Jie CHEN, Jia-Rui CHEN, Shou-Liang CHEN, Shu-Kun CHEN, Wen-Li CHEN, Yi-Lin CHEN, Zhi-Duan CHEN, Lun-Kai DAI, Yun-Fei DENG, Rui- Zhen FANG, De-Zhi FU, Yu-Ying GENG, Cui-Zhi GU, Li-Xiu GUO, You-Hao GUO, Ting-Nong HE, De- Yuan HONG, Qi-Ming HU, Chao-Mao HUI, Kai-Yong LANG, An-Ren LI, Bing-Tao LI, Heng LI, Pei-Qiong LI, Xi-Wen LI, Song-Jun LIANG, Qi LIN, Qi-Xin LIU, An-Min LU, Lian-Li LU, Ling-Di LU, Jin-Shuang MA, Hua PENG, Hua-Xing QIU, Hai-Ning QIN, Ya TANG, Wen-Cai WANG, Yin-Zheng WANG, Fa-Nan WEI, De-Lin WU, Nian-He XIA, Qi-Bai XIANG, Fu- Wu XING, Qin-Er YANG, Yong YANG, Jun-Sheng YING, Hong-Da ZHANG, Ji-Min ZHANG, Mei-Zhen ZHANG, Yong-Tian ZHANG, Zhi-Yun ZHANG, Shi- Dong ZHAO, Xiang-Yun ZHU, and Xuan ZHUANG. We would like to thank Anne BJORKMAN at the University of British Columbia for editing of the manuscript language. We would also like to thank Chelsea Rachel NAGY, Dr. Xiang-Cheng MI, and two anonymous reviewers for their helpful comments on the manuscript. This project was financially supported by grants from the National Natural Science Foundation of China for Key Projects (No F1001) and the Ministry of Science and Technology of China (No. 2007BAC03A08-8). References Fig. 7. Relationship between the proportions of endemism of different life form groups and altitude. Anderson S Area and endemism. The Quarterly Review of Biology 69:

12 92 Journal of Systematics and Evolution Vol. 49 No APG An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141: Axelrod DI, Al-Shehbaz I, Raven PH History of the modern flora of China. In: Zhang A, Wu S eds. Floristic characteristics and diversity of east Asian plants. Beijing: China Higher Education Press Balmford A, Green RE, Jenkins M Measuring the changing state of nature. Trends in Ecology & Evolution 18: Bretz F, Hothorn T, Westfall P Multiple comparisons using R. Boca Raton: CRC Press. Brooks TM, Mittermeier RA, da Fonseca GAB, Gerlach J, Hoffmann M, Lamoreux JF, Mittermeier CG, Pilgrim JD, Rodrigues ASL Global biodiversity conservation priorities. Science 313: Brown JH Macroecology. London: The University of Chicago Press. Brummitt N, Lughadha EN Biodiversity: Where s hot and where s not. Conservation Biology 17: Burke A Plant endemism in the central Namib Desert. Evolutionary Ecology Research 9: Cain SA Foundations of plant geography. New York: Harper. Casazza G, Zappa E, Mariotti MG, Medail F, Minuto L Ecological and historical factors affecting distribution pattern and richness of endemic plant species: The case of the Maritime and Ligurian Alps hotspot. Diversity and Distributions 14: Colwell RK, Hurtt GC Nonbiological gradients in species richness and a spurious Rapoport effect. American Naturalist 144: Colwell RK, Lees DC The mid-domain effect: Geometric constraints on the geography of species richness. Trends in Ecology & Evolution 15: Compilation Group of Study of China s Biodiversity China s biodiversity: A country study. Beijing: China Environmental Science Press. Cox CB, Moore PD Biogeography: An ecological and evolutionary approach, 7th ed. London: Bath Press. Cramer MJ, Willig MR Habitat heterogeneity, species diversity and null models. Oikos 108: Crisp MD, Laffan S, Linder HP, Monro A Endemism in the Australian flora. Journal of Biogeography 28: Cyranoski D Visions of China. Nature 454: Editorial Committee of China s Physical Geography China s physical geography physiognomy. Beijing: Science Press. Editorial Committee of China s Physical Geography China s physical geography. Beijing: Science Press. Editorial Committee of Flora Reipublicae Popularis Sinicae Flora Reipublicae Popularis Sinicae. Beijing: Science Press. Editorial Committee of Flora Reipublicae Popularis Sinicae Flora Reipublicae Popularis Sinicae. Vol. 1. Beijing: Science Press. Editorial Committee of Higher Plants of China Higher plants of China. Qingdao: Qingdao Press. ESRI ArcGIS 9.0. New York: ESRI Press. Everitt B, Hothorn T A handbook of statistical analyses using R. Boca Raton: Chapman & Hall/CRC. Feng Y, Pan B-R Study on floristic and ecology of species endemic to Xinjiang. Acta Botanica Yunnanica 26: Fu L-G, Feng Z-J, Zhuang J-Y, Ying J-S Species diversity. In: Chen L-Z, Wang X-P, Wang S eds. Biodiversity in China: Status and conservation strategy. Beijing: Science Press Fu Z-J Study on endemic phenomena of the flora in Qinling Mountain Range. Journal of Xinyang Teachers College (Natural Science Edition) 12: Gaston KJ Biodiversity: A biology of number and difference. Oxford: Blackwell Science. Gaston KJ Global patterns in biodiversity. Nature 405: Gaston KJ, Blackburn TM The spatial distribution of threatened species: Macroscales and New World birds. Proceedings of the Royal Society of London Series B-Biological Sciences 263: Good R The geography of the flowering plants. 4th ed. London: Longman. Groombridge B, Jenkins MD Global biodiversity: Earth s living resources in the 21st century. Cambridge: World Conservation Press. He F-L, Legendre P, LaFrankie JV Spatial pattern of diversity in a tropical rain forest in Malaysia. Journal of Biogeography 23: He J-S, Ma K-P Species diversity. In: Jiang Z-G, Ma K-P, Han X-G eds. Conservation biology. Hangzhou: Zhejiang Science and Technology Press Heywood VH, Watson RT Global biodiversity assessment. Cambridge: Cambridge University Press. Hu S The Metasequoia flora and its phytogeographic significance. Journal of the Arnold Arboretum 61: Jansson R Global patterns in endemism explained by past climatic change. Proceedings of the Royal Society of London Series B Biological Sciences 270: Jenkins M, Green RE, Madden J The challenge of measuring global change in wild nature: Are things getting better or worse? Conservation Biology 17: Jenks GF The data model concept in statistical mapping. International Yearbook of Cartography 7: Jin S-Y Compilation of type specimen of higher plant of China. Beijing: Science Press. Jin S-Y Supplements of compilation of type specimen of higher plant of China. Beijing: Chinese Forestry Press. Kessler M Upslope-directed mass effect in palms along an Andean elevational gradient: A cause for high diversity at mid-elevations? Biotropica 32: Kessler M The elevational gradient of Andean plant endemism: Varying influences of taxon-specific traits and topography at different taxonomic levels. Journal of Biogeography 29: Lamoreux JF, Morrison JC, Ricketts TH, Olson DM, Dinerstein E, McKnight MW, Shugart HH Global tests of biodiversity concordance and the importance of endemism. Nature 440: Latham RE, Ricklefs RE Continental comparisons of temperate-zone tree species diversity. In: Ricklefs RE,