An insight into the most threatened fl ora of China

China harbors a very rich plant biodiversity both in total number of taxa and in endemism. Nevertheless, a signifi cant fraction of this diversity (up to 20% of the native plants to China) is currently threatened. Among this endangered fl ora, an appreciable but still unquantifi ed number of taxa are in an extreme situation of risk because of their low population sizes, often consisting of fewer than 100 individuals. We have selected 20 plant taxa as a sample of this extremely threatened fl ora, and, from these, information about their geographic range, population size, threats, existing conservation measures, legal status and threat degree (according to the IUCN criteria) is provided. The extreme rarity of these taxa can be linked to their evolutionary history (they are palaeoor neoendemics) and/or to severe human disturbance (mostly habitat destruction and overexploitation) affecting them.


CHINESE FLORA: VERY DIVERSE BUT ENDANGERED
China is one of the richest countries of the world in terms of plant biodiversity, with more than 30,000 vascular plant taxa, and a very high endemism rate which might surpass 50% (SEPA, 1998;López-Pujol et al., 2006;CSPCEC, 2008).A growing fraction of this diversity is, unfortunately, threatened by extinction, and some authors have reported a number of endangered species ranging from 3,000 to 5,000, i.e. up to 20% of the total fl ora (Wang, 1992;Gu, 1998;Zhang, 2007;CSPCEC, 2008).However, and according to more recent studies (Wang & Xie, 2004;Xie & Wang, 2007), this fi gure could be even higher.For instance, from the ca.4,200 angiosperm taxa (i.e.just 14% of the total number of angiosperms in China) assessed in the fi rst phase of the elaboration of the China Species Red List (Wang & Xie, 2004;Xie & Wang, 2007), over 3,600 (87%) were regarded as threatened following the 2001 IUCN criteria (CR, EN, or VU), and up to 651 were assigned to the CR (Critically Endangered) category, that is, facing an imminent risk of extinction.
These large-scale evaluations of the Chinese fl ora, in addition to other studies (Gu, 2003;Cicuzza et al., 2007;Olfi eld & Eastwood, 2007), have pinpointed the existence of an appreciable, but still unquantifi ed, number of Chinese plants in an extreme situation of risk, taxa typically with one or very few (2)(3) localities and total population sizes consisting of a few dozens of individuals or even fewer.In fact, China probably harbors the most rare and endangered conifers in the world (e.g.Cupressus chengiana var.jiangeensis and Abies beshanzuensis var.beshanzuensis, from which only one and three individuals are remaining, respectively; see Appendix 1), but also angiosperms (e.g.Carpinus putoensis, Gleditsia japonica var.velutina, and Acer yangbiense, with just one, two and four individuals remaining in the wild, respectively; see also Appendix 1).Unless effective conservation measures are taken, these very rare and endangered taxa are condemned to disappear from nature in the near future.
Extinction seems to have occurred for several plant species whose status in the wild was reported as very endangered just a few years ago, such as Betula halophila or Cystoathyrium chinense (Zhang & Ma, 2008).In addition, other more common taxa have suffered a process of fast rarifi cation in recent years and today qualify as CR under criterion D (less than 50 individuals remaining in the wild).For example, Picea neoveitchii was "only" classifi ed as VU (Vulnerable) in the China Species Red List (Wang & Xie, 2004) which was compiled during the period 2000-2003; currently, this species may have less than 20 individuals remaining, and should be undoubtedly included within the CR category (Zhang, 2007).

A S E L E C T I O N O F T H E M O S T ENDANGERED CHINESE FLORA
Based on the current knowledge, we have elaborated a list of 20 plant taxa as a sample of the extremely endangered fl ora of China (Appendix 1).Being aware of the still relatively poor taxonomic and chorological knowledge of the Chinese fl ora, the taxa presented here do not represent in any case a complete, "closed" list of the most threatened plants, which is beyond the scope of this paper.Instead, we are aimed to refl ect the very critical situation of a growing number of plant taxa in China, which may soon disappear from the wild.
Only those plant taxa with an agreed taxonomy have been selected, and the main groups of vascular plants (ferns, gymnosperms and angiosperms) are all represented.In addition to taxa facing an extremely high risk of extinction in the wild (those classifi ed as CR), examples of species recently extinct in the wild (EW) have also been included.Information about their geographic range (Appendix 2), population size (total number of individuals of the taxon), ecology, threats, and existing conservation measures have been gathered for all the 20 taxa.In addition, their vernacular names, both in jianhuazi (simplifi ed Chinese characters) and pinyin (romanization system for Chinese), the synonymy, and a brief description of the plant have also been included.Finally, their legal status and threat degree (according to the IUCN categories) are also provided (Appendix 3).

ENDEMISM VS. HUMAN THREATS AS CAUSES OF ENDANGERMENT
The occurrence of many such cases of extremely rare and endangered plants in China, well exemplifi ed by the 20 taxa selected here (Appendix 1), can be explained by both natural and human-induced factors, in many cases acting synergistically.Most of these plant taxa were probably already rare well before the human activities began to seriously impact the Chinese natural ecosystems (i.e."naturally rare" plant taxa).In this case, the evolutionary history of plant species can explain, at least in part, their current extremely scarce distribution.Compared to other regions in the world, China is plenty of relict lineages (e.g.Qian & Ricklefs, 1999;Qian, 2001), which had a widespread distribution in the past but that the late Tertiary and Quaternary climatic deterioration caused their local extinction from many areas and their confi nement to favorable enclaves (the so-called "glacial refugia"), surviving in small and isolated populations.
Although not so well known as Cathaya, Ginkgo, Glyptostrobus or Metasequoia, most of the taxa contained in Appendix 1 are likely paleoendemics which have suffered severe contractions of their former distribution areas.
Pleistocene glacial refugia, in addition to be suitable areas for the persistence of ancient lineages during the Quaternary, also served as centres of plant evolution and diversifi cation (Tzedakis et al., 2002).Thus, the rarity of some plants should be explained, instead, by the lack of enough time to spread from their centres of origin (i.e.neoendemisms).From Appendix 1, this can be the case of Sinojackia sarcocarpa, a currently speciating taxon according to Yao et al. (2008).Notoriously, all the 20 plant taxa compiled here are exclusively located in central and southern China (see Appendix 2), where the existence of numerous and extensive Quaternary plant glacial refugia has been hypothesized (e.g.Ying et al., 1993;Wang & Liu, 1994;López-Pujol, 2008).
The large-scale human-mediated modifi cation of the environment in China, especially intensifi ed from the 1950s, has undoubtedly put a lot of pressure on plant biodiversity (e.g.Liu et al., 2003;López-Pujol et al., 2006).Obviously, the impact has been more severe on the plants which were already rare, pushing them to the brink of extinction or even producing their extirpation from nature.In fact, it is thought that at least 200 plant taxa have become extinct from the 1950s (Zhang et al., 2000), most likely due to habitat destruction, fragmentation or deterioration.To our knowledge, dam building (an extreme case of habitat destruction) has caused the extinction of at least two plant species in China because their populations were located in the areas to be fl ooded: Rhododendron kanehirai, in Taiwan Island (IUCN, 2008), and Plantago fengdouensis (Appendix 1), in the Three Gorges Reservoir Region.
The critical situation for most of the plant taxa included in Appendix 1 is probably also a consequence of the destruction of natural ecosystems, sometimes combined with the overexploitation of these species.For example, habitat destruction is the main reason for the extirpation of Euryodendron excelsum from Guangxi Province (Appendix 1 and Fig. 1), which is at present surviving only in a small population in Yangchun County, in Guangdong (Shen et al., 2008).Picea neoveitchii, a taxon formerly present in up to 6 provinces according to Flora of China, has reached its current highly threatened status (only 11 mature individuals are remaining; Appendix 1) mainly as a consequence of the combination of overexploitation (due to its use as timber) and habitat fragmentation (Zhang, 2007).The massive collection of individuals because of their ornamental value has contributed to the fact that most of the Cycas species of China, including that present in Appendix 1, are today endangered (Donaldson, 2003).
Pollution has also contributed to the endangerment of rare species in China: the contamination and eutrophication of the aquatic habitats where the four Isoetes species native to China are living are among the main causes for the decline and loss of populations (Liu et al., 2005).For example, Isoetes yunguiensis (which is included in Appendix 1) has lost most of their former distribution area (it has been completely extirpated from Yunnan), and the only remaining population in Guizhou (with only about 50 individuals) is severely menaced by pollution and overgrazing (Liu et al., 2005;Chen et al., 2007).
In addition to human threats, stochastic events (such as a natural catastrophe) can cause the direct extirpation of these species from nature due to their extremely reduced number of populations and individuals (well below the minimum viable population size, MVP).For example, with Taiwan's 1999 earthquake, the unique population of Isoetes taiwanensis shrank from 5,000 to only 50 individuals, and its occupation area also diminished from 2,000 to <10 m 2 (Liu et al., 2005).Finally, the progression of climate change (global warming) may represent the coup de grâce for these extremely rare and endangered species.

CONSERVATION OF THE CHINESE EXTREMELY THREATENED FLORA
Although in China the conservation of nature can be traced back many centuries and even millenia, the "modern" conservation practices started late (mainly since the middle twentieth century), and were almost totally suspended during the convulse years of the Cultural Revolution (1966)(1967)(1968)(1969)(1970)(1971)(1972)(1973)(1974)(1975)(1976).However, from the late 1970s, and coinciding with the onset of the economic reforms, they received a new and defi nitive impulse, including those related to the rare and endangered fl ora (Gu, 1998;Xu et al., 1999;López-Pujol et al., 2006;Zhang, 2007).Regarding in-situ plant conservation, China has experienced an astonishing expansion of its network of protected areas in recent years, now covering more than 15% of the total land area.China has also implemented several ex-situ measures to protect its fl ora, such as the building of numerous botanical gardens and arboreta (ca.160), but also fi eld nurseries and plant introduction bases, which are assuring the conservation of more than half of the plants native to China (CSPCEC, 2008).In addition, fi eld work oriented to expand the chorological knowledge of the Chinese fl ora has experienced a great advance in recent years.For example, the populations of Apterosperma oblata discovered in recent years have increased the total population size of this endangered species from just a few individuals to more than one thousand (Yuan et al., 2007).
It should be noted that a significant fraction of the 20 extremely endangered plant taxa presented here are either included (partially or totally) within a protected area or cultivated (or their seeds preserved) in a botanical garden (see Appendix 1).It must be equally noted, however, that nature reserves in China are not always properly managed (mainly due to lack of funds and staff), and that both the sizes of the collections and the number of gardens where a given plant is cultivated are generally insufficient (Xu, 1997;Zhang, 2007).For example, the only ex-situ collection of Picea neoveitchii consist of two individuals cultivated in the Xi'an Botanical Garden (Zhang, 2007).
In addition to in-situ and ex-situ conservation measures, a lot of environmental legislation has been promulgated in the last two decades in China (as restrictive as European in many aspects but with many problems related to its enforcement still remaining), including some protection lists for rare and endangered species: the National List of Rare and Endangered Plant Species (issued in 1984), from which the China Plant Red Data Book (Fu, 1992) was later released, and the fi rst batch of the Catalogue of the National Protected Key Wild Plants (1999) under the Regulations on Protection of Wild Plants (1997), which contained about 300 strictly protected plant taxa (Zhang & Ma, 2008).Despite the extremely endangered fl ora of China (exemplifi ed by the taxa included in Appendix 1) is mostly included in these protection lists (Appendix 3), some of the theoretically protected taxa still lack of effective conservation measures, and even a few seem to have disappeared from the wild, such as Cystoathyrium chinense, Betula halophila, or Betula jinpingensis (Zhang & Ma, 2008).
Fortunately, most of these defi ciencies in plant conservation are in the way to be corrected.The recently launched China's National Strategy for Plant Conservation will mean a great improvement both in the in-situ and ex-situ conservation of plant species (CSPCEC, 2008).Moreover, the implementation of comprehensive conservation and/or restoration programs for endangered plants has also taken root in China during the last few years: these have allowed, for example, the effective protection of the populations of Myricaria laxifl ora and Adiantum reniforme var.sinense to be fl ooded by the Three Gorges Reservoir (through ex-situ cultivation and further translocation to the fi eld; Kang et al., 2006;Liu et al., 2006).For some of the taxa included in Appendix 1 (and even for plants not still legally protected, e.g.Acer yangbiense) conservation measures beyond mere inclusion in nature reserves or cultivation in botanical gardens are underway or projected, in order to assure their long-term viability.For example, a reinforcement program for Pachylarnax sinica (=Manglietiastrum sinicum), a Magnoliaceae with only about 50 individuals remaining in the wild, has completed its fi rst stage with a notable success: about 200 saplings (coming from local nurseries which have produced over 5,000 young trees) were introduced in 2007 in its population of Xiaoqiaogou Nature Reserve, with survival rates of ca.90% (GTC, 2008).A restoration program has also been planned for Acer yangbiense (Fig. 1) in order to increase its current population size (only 4 individuals; BGCI, 2008a).In other cases, urgent and drastic measures have had to be taken in order to save plant species from their imminent extinction, e.g.Plantago fengdouensis.All the living individuals of this species endemic to the Three Gorges Reservoir Region were transplanted to a botanical garden before the fl ooding of its natural populations (People's Daily, 2008).
The accumulated experience from these ongoing or already completed conservation and restoration programs should be applied to those threatened species still lacking effective preservation measures, in order to prevent further decline.To our knowledge, insuffi cient or no in-situ and ex-situ conservation measures have been implemented for several plant taxa from Appendix 1 (for example, up to eight taxa appear not to be cultivated in botanical gardens), a fact which may be behind their rarefaction or even their putative extinction (e.g.Craigia kwangsiensis).It is also highly advisable that the forthcoming protected plant lists include the obligation to develop and implement management and/or recovery programs (for at least the most endangered taxa, as occurs in some countries such as the United States).These programs, in addition to comprise "classical" tools (e.g.establishment of plant reserves, population monitoring, seed collection, education and outreach), should also include the most novel approaches in conservation biology, such as DNA banking (Dulloo et al., 2006).

Figure 1 .
Figure 1.Some of the most threatened plant taxa of China: (A), Cultivated individual of Cupressus chengiana var.jiangeensis in Mendocino Coast Botanical Garden (California, USA) [Picture: Chris Woods]; (B), Several individuals of Pinus squamata in its natural habitat [Picture: Zhi-Yong Zhang]; (C) and (D), Leaves and fruits of a wild individual of Acer yangbiense [Pictures: Yousheng Chen]; (E) and (F), wild individual of Euryodendron excelsum, and greenhouse cultivated ones [Pictures: Shen Shikang]; (G), Cultivated individual of Magnolia zenii in University of British Columbia Botanical Garden (British Columbia, Canada) [Picture: Daniel Mosquin].