Orchid diversity in China ’ s Hainan Island : Distribution and conservation

Orchid diversity in china’s hainan island: distributiOn and cOnservatiOn.— Orchidaceae are widely distributed in many terrestrial ecosystems except for polar and desert areas and constitute a “flagship group” in biological conservation. As the largest tropical island of China, Hainan has five tropical forest vegetation types, namely deciduous monsoon forest, lowland rainforest, montane rainforest, montane evergreen forest, and montane cloud forest. There are 317 orchid species in the island, including 33 endemic, 158 epiphytic, 148 terrestrial, and 11 saprophytic species. Most orchids, which are mainly located in central and southern parts of the island, are generally distributed in damp tropical forests in mountains at an altitude of 500–1500 m. Highest level of endemism is also centred in these areas. Orchids are especially threatened by habitat fragmentation because they grow in small populations, and fragmentation may block gene flow and result in lower genetic diversity. In addition, due to their ornamental and medicinal value, many orchids are over-collected. Therefore, orchid conservation in Hainan Island is very urgent. The aim of this article is to determine the distribution pattern of orchids and expound research and conservation status in Hainan Island, and to propose conservation strategies for the future.


INTRODUCTION
As one of the largest angiosperm families, Orchidaceae contains about 870 genera and 27,000 species (Cribb et al., 2003).The family is widely distributed in a variety of terrestrial ecosystems (especially in tropics), although it is absent from polar and desert areas (Romero, 1996).As a result of the long evolution, in the family Orchidaceae the flower structure has become highly specialized and breeding systems have also actively evolved, so it is considered as one of the most advanced families within the angiosperms (Chen & Luo, 2003).Orchids have highly specialized pollination systems; about 60% of orchids present only one pollinator (Cingel, 2001).For this reason, they are also considered a model to illustrate the important role of pollinators in plant species differentiation (Tremblay et al., 2005).If compared with other families, orchids' complex life-history and special habitat requirements (Fay & Chase, 2009;Schödelbauerová et al., 2009), together with the fact that most species show small populations and a narrow-pattern distribution (Chung et al., 2005;Rodrigues & Kumar, 2009), make them more vulnerable to the threats derived from habitat loss and degradation (Coates & Dixon, 2007;Swarts & Dixon, 2009).Furthermore, because most orchids have high ornamental and medicinal value, over-collection has become another significant threat to the survival of Orchidaceae (Hágsater & Dumont, 1996;Koopowitz et al., 2003).All wild orchids in the world were included into the scope of Convention on International Trade in Endangered Species (CITES), accounting for more than 90% of plants that should be protected based on this convention.Thus, the Orchidaceae should be regarded as a "flagship group" in biological conservation (Luo et al., 2003).
In Hainan, orchid species are distributed in various forest types (Wang, 2004;Song, 2005;Yu, 2006;Liu et al., 2010;Wu, 2013;Yang, 2013;Zhang, 2013;Hu, 2014).Hainan Island, the largest tropical island of China, has a diverse tropical rainforest including deciduous monsoon forest, lowland rainforest, montane rainforest, montane evergreen forest, and cloud forest.Hainan has a rich biodiversity and it is one of the most valuable areas for biodiversity conservation not only in China but also among the world's tropical rainforest areas (Sun et al., 1999).
In this article, we aim to determine the orchids' distribution pattern and to identify the diversity and endemic centres in Hainan Island.We will also introduce the state-of-the-art of the research and conservation status of Hainan's orchids, in order to discern whether or not the location of the current nature reserves is reasonable.Furthermore, according to the data collected, we propose conservation strategies for the future.

SpeCIeS DIveRSITy AND DISTRIbUTION pATTeRN
There are 102 genera and 317 orchid species distributed in Hainan Island (Table 1), including 33 endemic species of this area, 158 epiphytic species, 148 terrestrial species, and 11 saprophytic species.This area has only less genera than Yunnan, and less species than Yunnan and Taiwan provinces (Table 2).However, the species density of Hainan Island is the highest among the five provinces included within the tropical regions of China.
Geographic distribution of orchids tends to be not homogeneous.Both the species diversity and endemism centres are located in the central and southern parts of the island, which are mountainous regions.Species in Baoting, Lingshui and Sanya counties account for more than 80% of the total number in Hainan Island (Fig. 1).This region is the main centre of diversity and has a very high value for protection.Benefited from the humid and warm environment, more epiphytic than terrestrial orchids are found in most of the counties in Hainan Island.However, there are still five counties with more terrestrial orchids than epiphytic species, namely Dongfang, Haikou, Lingao, Tunchang, and Wenchang (Fig. 1).
The concept "species irreplaceability" first came up in Pressey et al. (1994).If a species is found in more than one area, these areas have low irreplaceable value; conversely, if a species is found only in one area as an endemic species, the irreplaceabil- ity is 100% (Pressey et al., 1994).When species are threatened, such areas should have priority for protection.Numbers of endemic species in Baoting, Lingshui and Sanya are the highest in Hainan Island (Fig. 2) and thereafter irreplaceability of the three areas is quite high.Besides, these areas are very rich in species and consequently they deserve the highest priority for protection.

HAbITAT AND pOpUlATION STATUS
In Hainan Island, orchids are mainly distributed in tropical forests of mountains at an altitude of 500-1500 m.There are a lot of epiphytic orchids in the tropical forests.Epiphytic orchids mainly grow on the trunks or branches of tall trees.Many populations of wild orchids are small, and easily destroyed by habitat fragmentation.As a result, recruitment of new individuals in populations is diminished.Until now, specific research in population dynamics has been carried out in several orchid species such as Dendrobium sinense Tang & F. T. Wang (Wu, 2013), Paphiopedilum appletonianum (Gower) Rolfe (Chen et al., 2009), and Phalaenopsis pulcherrima (Lindl.)J. J. Sm.(Yang, 2013), and all these works indicated that wild populations were experiencing a rapid decline.

GeNeTIC DIveRSITy
The conservation of biological diversity is ultimately depending on the preservation of genetic diversity (Wang & Hu, 1996).Since the basic unit of evolution is the population (Dobzhansky, 1937;Stebbins, 1963), genetic diversity studies must be focused on genetic diversity at the population level.However, currently, research on the genetic diversity of Orchidaceae in Hainan Island is still limited.There are some researches in Dendrobium and Oncidium (Ren et al., 2007(Ren et al., , 2008(Ren et al., , 2013)), but they are at the species level.The only report on population genetic diversity is about Phalaenopsis pulcherrima (Hu, 2014).Thus, there is still an important lack of information on the genetic diversity of Orchidaceae in Hainan Island, especially at the population level.Genetic diversity is the basis for the identification of key spots that need to be protected, and also the intuitive manifestation of the population adaptability and evolutionary potential.Therefore, it is extremely urgent to carry out new research on genetic diversity at the population level.

THReATS AND CONSeRvATION STATUS
Many orchids are specialists depending on only one (or a few) mycorrhizal fungi and pollinators.This specificity added to its narrow range and small population sizes make orchids especially vulnerable to climate change, human disturbance, and habitat fragmentation.Furthermore, many orchids have high ornamental (Hu, 2014) and medicinal value (Wu, 2013).For these reasons, orchids have been excessively collected and seriously destroyed in Hainan Island (Hu, 2014).
In situ conservation is aimed to protect wildlife in their natural habitats, which ensures the maintaining of ecological processes and the ongoing processes of evolution.At present, there are ten National Nature Reserves established in Hainan Island, namely Yinggeling, Bawangling, Jianfengling, Tongguling, Wuzhishan, Diaoluoshan, Datian, Dongzhaigang,  , 2012).Except for the last three marine natural reserves, orchids are found in the other seven nature reserves (Yu, 2006;Wu, 2013;Yang, 2013;Zhang, 2013;Hu, 2014).However, no national nature reserves have been established in Baoting, Lingshui and Sanya counties, where many orchids are distributed (Figs. 1 and 2).It is urgent to establish new nature reserves at the appropriate level in these three areas where orchid diversity is high.Nevertheless, many requirements should be met to establish a nature reserve.Besides, ex situ conservation can be used as a complementary method for orchid conservation.In the context of ex situ conservation, the endangered orchids can be transferred to new locations for special protection and management, including botanical gardens or "endangered species breeding centers", in order to increase their probabilities of survival and reproduction.
At present, the main method of ex situ conservation of Orchidaceae in Hainan Island is the establishment of nurseries through tissue culture, and current research focuses on the study of mycorrhizal biology to improve seedlings' survival rate in several species, including Dendrobium loddigesii Rolfe, Dendrobium nobile Lindl., Dendrobium sinense, and Phalaenopsis pulcherrima (Ke et al., 2008;Zhou et al., 2009;Chen et al., 2010bChen et al., , c, 2011;;Cui & Song, 2011;Li et al., 2011).However, we should be aware that ex situ conservation is not a "natural" protection.Only if introduced into their natural habitat (i.e.reintroduction) the individuals can evolve naturally, which ensures species long-term survival (Chen et al., 2010a).The only reported reintroduction was that carried out with Dendrobium sinense (Yang, 2013).In sum, ex situ conservation of orchids in Hainan Island needs considerable work, especially concerning reintroduction.

Genetic diversity of orchids
Establishment of natural reserves should not be only based on genetic and species diversity but also on ecological diversity.Because it is not possible to comprehensively assess the genetic diversity of over 300 orchid species in a short time, priority should be given to a smaller set of species.The most endangered, rare and regionally unique species should be in the front row for molecular studies on population genetic structure.Populations with higher genetic diversity should be protected with in situ methods such as establishing natural reserves, whereas conservation of populations with lower genetic diversity should be complemented with ex situ conservation measures (such as artificial breeding and reintroduction techniques).

Origin and evolution of island endemic species
In Hainan Island up to 397 endemic species have been recorded so far (Francisco-Ortega et al., 2010).Due to the importance and irreplaceability of endemic species, it is urgent to carry out studies on their speciation mechanisms and evolutionary trends.In general, both extrinsic and intrinsic factors can accelerate speciation and evolution of endemic species.An important external factor could be, for example, the blocking of gene flow via pollinators.If gene flow is restricted for long periods of time, different species could be originated.On the other hand, the occurrence of gene mutations is an intrinsic factor that could also result in speciation.Achieving a better knowledge of mechanisms and evolutionary trends will allow us to design more suitable tools to protect plant biodiversity.

Conservation through artificial propagation and reintroduction
Regions with low species diversity of orchids in Hainan Island are not among the best candidates to be covered by nature reserves, as occurs elsewhere.In this case, ex situ conservation is probably the only option to reduce the declining of populations or endangered species.Plants can be taken back to the breeding bases and nurseries to propagate them with tissue culture methods and the use of mycorrhizal interactions.Tissue cultured experiments of artificial hybridization can also be carried out in plantlets for improving diversity.When the conditions are appropriate, these plants can be reintroduced into their natural habitats.Therefore, large-scale propagation and mycorrhizal biology research of orchids should become one the most urgent and important issues regarding their conservation.In addition, the reintroductions should be combined with population genetics research to assess adaptation after reintroduction.Orchid diversity in China's Hainan Island

Working with conservation organizations and local governments or communities
The scientific and feasible approaches to strengthen conservation of orchids in Hainan Island are important.What is more, there should be some regulations to solve the problem that local people collect orchids excessively to pursuit the profit stemming from the high ornamental and medicinal value of these plants.We must also take some non-academic actions to collaborate and co-work with local governments, communities and NGOs to promote the conservation of orchids.

Figure 1 .
Figure 1.Distribution pattern of wild orchids in Hainan Island.For the names of the administrative divisions of Hainan, see Fig. 2. Codes of the provinces in the inset map: GD, Guangdong Province; GX, Guangxi Province; HN, Hainan Island; TW, Taiwan Island; YN, Yunnan Province.

Table 1 .
Orchid genera and species numbers in Hainan Island, China.

Table 2 .
Comparison of orchid species richness in Hainan Island and in neighboring areas.