Heptacodium miconioides is a deciduous tree species with a restricted distribution in East China. This species is a well-known ornamental or horticultural plant, and has been listed as endangered (Chen, 1993). During early May, the glossy leaves emerge and remain attractive throughout the season. In late summer, creamy white, jasmine like blossoms emerges from the tips of the branches while few other woody plants are in bloom. The blooms are sweetly fragrant and persist for several weeks. In early fall, the flowers mature and develop small, inconspicuous fruits surrounded by a persistent calyx. When the calyces turn a bright cherry red, it forms another spectacular, eye-catching landscape. Even during winter with flowers and foliage absent, the plant is still of ornamental values with its light brown bark. H. miconioides occupies a very important position in the evolutionary history of the Caprifoliaceae. Because its morphological characteristics are intermediate between Caprifoliaceae and Linnaeeae, there ever were hot disputes about its phylogenetic position (Fukuoka, 1972; Donoghue, 1983; Xu, 1983; Takhtajan, 1987; Tang et al., 1994; Mabberley, 1997). Recently it is confirmed by the molecular phylogenetic studies (Backlund et al., 1998; Pyck et al., 2000).

Due to environmental deterioration and human disturbance, its habitat has been destroyed and fragmented continuously. At present, studies about H. miconioides have been launched from many aspects. In the field of ecology, Chen(1994) studied ex suit conservation of H. miconioides at the earliest, and then Liu(1999a; 1999b; 2003), Jin(1997; 1998; 2004) and Hao(2005b; 2006b) conducted systematic and overall researches. Recently Chen et al.(Li et al., 2004). also showed interest in this plant. Those scholars have studied ecological characteristic of its community and population, physiological response to light stress, photosynthetic characteristics, approach and method for its conservation, reproductive biological characteristics and the genetic diversity and variation and so on.

1 Distribution and resources

H. miconioides is restricted in a small geographic range in the subtropical montane forests in East China where rainfall is not less than 1 000 mm per year. H. miconioides prefers the humid sites along the escarpments and the ravine, with soil humidity and relative elevation being important predictors (Liu et al., 1999a; 1999b). This species is distributed on all the facing aspect between 400 and 1 300 m, and mostly between 650 and 950 m above sea level. The flora of the region belongs to the east Asia zone and represents the feature of transition from subtropics to warm temperate area, and the vegetation types are mainly composed of evergreen broad-leaved forest, semi-evergreen broad-leaved forest, mixed coniferous and broad-leaved forest and deciduous broad-leaved forest. In these forests Lindera glauca, Cyclobalanopsis glauca, Fraxinus retusa, Alniphyllum fortunei, Cyclocarya paliurus, Sapium japonicum and the like are dominant or co-dominant species (Yu et al., 2003).

The remnant populations of H. miconioides are mainly distributed in Zhejiang Province, such as Dapan Mountain, Changhua County, Dongbai Mountain, Bei Mountain and Tiantai Mountain, and are sporadic in Jing County and Xuancheng County of Anhui Province (Zhang et al., 1993). In recent decades, its populations have declined rapidly and even disappeared at some locations. Yu et al. (2003) investigated its geographical distribution in Zhejiang Province and found the occurrence of H. miconioides in Xianju County (28°28′09″-30°16′11″N, 119°02′40″-121°11′44″E) for the first time, but they couldn't find it in Jiande County, Jinyun County, Zhuji County and Shengzhou County where it had been recorded. The total area of H. miconioides forests in Zhejiang is 54.28 hectare, which is mainly composed of three island regions: Changhua in Northwest Zhejiang, Tiantai Mountain and Kuocang Mountain in East Zhejiang.

2 Causes analysis on endangering of H. miconioides

The endangering causes of plants are various, such as climatic change, human disturbance and its characteristics, and are often interactive rather than isolated (Oldfield et al., 1998). Some factors are extrinsic to the life history of the species in its native habitat (e.g. habitat destruction, exotic competitors and predators, and lack of pollinators), while others are intrinsic and reflect fundamental biological attributes that may constrain distribution and abundance (Pavlik, 1994). When efforts are made on its conservation and recovery, it is important to assess main factors that result in the decline of its population. In this paper, we reviewed our and other scholars' studies to analyze the endangering causes and conservation strategies of H. miconioides.

2.1 Migration during the climatic changes in history

We have gotten some data about the divergence time of Heptacodium. Ozaki (1980) identified one fossil species (H. hokianum) of Heptacodium from the late Miocene in southwest Honshu, Japan. Tang et al. (1994; 1996) grouped Heptacodium as palaeoendemic genus based on three main attributes, and classified this genus as the Tethyan Tertiary element. In case of having no direct fossil evidence, researchers can generally analyze the divergence time of plant species according to palaeoclimate conditions in its distributive place and its ecological demands (Wang, 1989). The modern distribution center of H. miconioides is restricted in a small geographic range of Zhejiang Province, Southeast China, with high humidity being important predictors. The researches on Chinese palaeogeography indicated that Southeast China belonged to the subtropical arid land from late Cretaceous to Paleocene, and its climate transferred gradually to aridity and coldness after late Miocene (Wolf, 1978; Tao, 1992). Both were not climate types suitable for H. miconioides and couldn't offer climatic conditions for its origination. Whilst, since late Tertiary, paleoenvironmental changes, especially the uplifting of Himalaya Mountains and Qinghai-Tibet Plateau, changed greatly the former terrain and then climate type (Zhou, 1982). With the South humid zone expanding northwards and the Pacific Ocean humid zone strengthening, the climate conditions in distributive place of H. miconioides changed from cold aridity to warm humidity (Frakes, 1979). This climate type was similar with ecological demands of H. miconioides. Based on the analysis above, it would be reasonable for its divergence time to be between the Paleocene and Early Miocene.

Plant migration in history was a very real phenomenon with evidences of prehistoric and present observations (Pitelka et al., 1997). During this course, large quantities of plants were extinct for their feeble adaptability to the climatic changes, and some succeeded in migration and survived. Therefore the modern distribution of plant species was determined by their reflection not only to habitat conditions, but to climate, landform during the prehistoric period (Wolf, 1964). During the divergence time of H. miconioides (the Paleocene and Eocene), the global temperature was warm and stable, and rainfall increased acutely to the highest point. This species had been adapted to the humid and warm climate conditions. With the temperature decreasing, H. miconioides had to begin the migration southwards. When the temperature increased in the interglacial, this species could not endure rising of temperature and had to migrate northwards again. In short, strong climatic changes in history perhaps resulted in a great decline of the population and a massive shrinkage of the distribution range, which might be the main cause for its habitat fragmentation and rare resources today.

2.2 Human disturbance

It is clear that most of H. miconioides populations have undergone the human disturbance in different degrees. This species has been harvested as firewood for a long time, and this kind of activities is not completely ceased even in recent years (Hao et al., 2003). In the forests, its individuals, even some large ones, are usually suckers from stump. Although strong sucking ability can counteract the effect of logging on its populations to a certain extent, deforestation led to death of some individuals and poor natural regeneration (Hao et al., 2006a). Investigation on its field populations showed that well-conserved populations in Zhejiang, such as populations in Dapan Mountain and Tiantai Mountain, were all distributed in the remote and untraversed mountains. In those places, H. miconioides is found dominant or co-dominant species near the escarpments and the ravine with gentle slopes, low rock bareness and thick soil(Hao, 2005). Whilst in the populations often disturbed by human, its individuals are only distributed at the inaccessible escarpments or ravine, and almost disappear in the slope where has been planted tea or Chinese Fir (Cunninghamia lanceolata).

Moreover, human disturbance has destroyed habitat conditions of H. miconioides. Small forest fragments are exposed to great change in microclimatic condition because they have high proportions of edges (Raphael et al., 1999). An altered microclimatic environment around forest edges could directly influence plant reproduction and recruitment (Sizer et al., 1999; Scott et al., 2002; Tomimatsu et al., 2004). Fragmentation may also increase vulnerability to invasion by exotic species such as more entrance, for exotics as well as increased likelihood of their disturbance (Michelle et al., 2004). Some studies have been attempted to reveal the effect of habitat fragmentation on H. miconioides. Liu et al. (2003) investigated the physiological responses of H. miconioides at eight different sites under fragmental habitats in the Bei Mountain, and found that strong light brought by habitat fragmentation obviously inhibited the photosynthesis rates, reduced antioxidant enzymes activities, and promoted electrical conductivity and MDA content. Hao et al. (2006b) studied the caloric values of three tree species (H. miconioides, Lindera glauca, Glochidion puberum) in different habitats (inside forest, at edge of forest and outside forest) and found out that environment changes due to habitat fragmentation increased significantly the caloric values of the sampling species. These results showed that habitat fragmentation had an influence on survival of H. miconioides and even its evolution.

2.3 Biological and ecological characteristics 2.3.1 Special status in the forest

As a small tree species the average height of mature H. miconioides reaches only to 7~9 m lower than many other subtropical evergreen or defoliated plant species (Editorial board of flora of China, 1988), therefore most individuals are distributed in the shrub or sub-tree layer, little in the tree layer (Jin, 1998). Of its nineteen vegetation types analyzed (Yu et al., 2003), H. miconioides can become dominant or co-dominant species where its competitors are also shrub or small tree species, such as Lindera glauca, Weigela japonica. The researches on photosynthetic characteristics showed that H. miconioides seedlings in high shading habitat often died and seedling recruitment was rare because its adaptability to low intensity of illumination was weak (Ke et al., 2002; Liu et al., 2003). Its low photosynthetic rate, sparse canopy and short growth period limited the photosynthesis product accumulation and growth rate (Ke et al., 2002). The seedlings from seeds were seldom found, and clone was the primary way of population recruitment, but not enough (Li et al., 2004). The researches on diameter structures of different populations also supported this conclusion (Jin, 1997; Li et al., 2004; Hao et al., 2005a). The analysis above showed that the shady environment had negative influence on its population recruitment, so we can take the thinning of crown canopy to increase light transparence as one of the conservation strategies.

2.3.2 Sexual reproductive obstacle

Patterns of reproduction have important roles in determining the amount and distribution of plant species, and reproductive obstacle is one of important causes that can cause a species to become threatened or endangered. The reproductive biology data of H. miconioides indicated that self-pollination was high, which would depress the idioplasmic renewal. Only one third of pollens could germinate and fewer could reach ovary in which only one ovule developed, and the average seed-set from ovule was very low (only up to 10.8%) (Bian et al., 2002). The question of whether pollen or resource availability limits seed-set in nature has stimulated a number of field studies, even different studies on the same plant species have sometimes yielded opposite results (Pyke, 1982; Whelan et al., 1986). Bian's study (2002) showed that the low seed-set might mainly be caused by resource limitation, but the farther research was not consisted with the foregoing conjecture. The research on morphological variation of reproductive apparatus found no significant differences in the seed rates of H. miconioides in different habitats, and flowering thinning could improve the seed status indicating that H. miconioides had a poor nutrition adjustment by itself and the number of fruits produced might potentially be high (Bian et al., 2004). Low seed germination has been a problem in stand establishment of H. miconioides, however, the mechanism of seed dormancy and how to increase seed setting rate is still unknown.

The preliminary research showed that the embryo of adult germs were underdeveloped and its seeds need go through a long time (470~500 d) to end dormancy, which might be one of the major limiting factors for germination. In the course of dormancy, its seed bank will shrink for the animal's predation, rotten, and so on. Additionally, it is difficult for its seeds to germinate successfully in the special habitat (i.e. high rock bareness and thin soil), and germination rate of those seeds is low by only 5%~10% (Hao et al., 2003). Thus biological characteristics of H. miconioides, for examples, low ratio of seed setting, low ratio of germination and disadvantage of the seedling and juvenile, are main reasons for the failure of its sexual reproductive, and its populations have to depend on the clone recruiting (Li et al., 2004). This regenerative pattern will depress the idioplasmic renewal and limit the dispersal of its populations.

2.3.3 Genetic variation and erosion

Genetic pattern within a species is thought to be crucial for the long-term survival and continued evolution of populations or species (Huenneke, 1991). Thus an accurate estimate of the level and distribution of genetic diversity of threatened and endangered species is an important element in designing conservation programs (Hamrick et al., 1991). Some researchers have studied genetic diversity patterns of H. miconioides using random amplified polymorphic DNA (RAPD) markers.

Jin et al. (2004; 2005) analyzed genetic diversity patterns of 4 populations according to the size class and of 3 populations at different altitudes in Tiantai Mountain. The results showed that genetic variation existed within and among populations with different size class, but the genetic variation within populations was higher than that among populations. The distinct genetic variation existed among populations at three different altitudes in spite of the relatively small geographical distribution, and gene flow among these three populations was relatively weak. Li et al. (2005) and Hao et al. (2005a; 2005b) studied the genetic diversity and variation of its different populations sampled from Zhejiang Province. According to those studies, its populations were in lack of genetic diversities compared with other threatened or endangered long-lived plants (Zoller et al., 1999), and genetic variation is occurred mainly among rather than within populations. The genetic diversities of some populations with bigger sizes were detected more abundantly than smaller populations, which indicated unavoidable minimum of genetic diversity with the present population's size shrinking. Small population size and low genetic diversity will decrease ecological adaptive ability of H. miconioides. Furthermore, low genetic diversity, great reproductive obstacle and low competitive ability limited the development of its population, and finally formed a vicious circle making H. miconioides endangered.

3 Conservation strategies and suggestions 3.1 Biodiversity conservation education and forest law execution

Great efforts have been made to protect the natural environment and natural resources. The government has constituted Forest Law, Environmental Protection Law and many statutes about environmental conservation for a long time, and thus has established a legislation framework. But some people are still unaware of the significance of biological diversity, especially lack knowledge about consequences of genetic erosion and species extinction. Most local dwellers don't know H. miconioides, and furthermore can't understand its function and significance in the biological diversity conservation and sustainable development. Even if nowadays, there is still human disturbance in some populations, such as Dongbai Mountain, Beishan Mountain.

To ameliorate this status, we should adopt the following three strategies. Firstly, the local government should strengthen the relative training for workers. Then more local dwellers can realize and understand the significance of plant conservation by the propagation and education of those trained workers. Environmental education is of a very strategic and important role to solve the environmental problems. But now the education on the conservation of H. miconioides is far from the requirements. Secondly, forest department should reinforce publicity and execution of law and legislation. Only when those laws and legislations were executed effectively, could human disturbance be prevented. Lastly, the local government should develop the firewood forest to supply firewood for the local dwellers. And if permitted, the local government can help the dwellers build simple biogas digester instead of firewood.

3.2 Conservation strategies of H. miconioides

In situ conservation has been widely adopted as an important means for conserving rare and endangered plant species over the world. It is believed to be ecologically efficient because they protect both species and their habitats. Considering the population size, habitat conditions, genetic diversity and variation, in situ conservation will be suitable for populations in Dapan Mountain, Tiantai Mountain. Some small populations in better habitats shouldn't been ignored in an in situ conservation strategy. The recruitment of sexual seedlings is rare or sporadic, so it is necessary to enlarge the population size with artificial breeding technology. Some clone reproduction methods of H. miconioides have been researched, among which the technology of cutting reproduction has better maneuverability (Liu et al., 2001). We can use cutting seedlings to enlarge the population size. At the same time, ecological engineering should be introduced to restore and rehabilitate the damaged or degraded communities. This conservation strategy can maintain most resource and genetic diversity of H. miconioides. At present, establishment of nature reserve or spot is recommended as the main conservation strategy.

Although it is commonly accepted that the most effective and efficient mechanism for the conservation of biodiversity is habitat protection, it is acknowledged that ex situ conservation can be critical components of a comprehensive conservation program. Chen (1994) conducted a primary study on the ex situ conservation of H. miconioides and succeeded in transplanting a few individuals to Lushan Mountain Arboretum. In our opinions ex situ conservation would be feasible for some populations (e.g. Dongbai Mountain) where habitat conditions have degenerated and population size is small. These H. miconioides individuals can be transplanted to other populations or botanic garden which also provide important opportunities for public education.

Since gene flow can alleviate the problems associated with isolation of small populations, it is feasible to use artificial gene flow for conservation purpose. For instance, cutting seedlings or adult individuals from one large and vigorous population can be cross-transplanted to a small and endangered population to increase its genetic diversity. We can also use cutting seedlings from different populations to construct new populations in the field.

3.3 Some aspects requiring to be researched

Sexual reproduction of plant can not only maintain natural renewal of the populations, but increase their genetic diversities. There is obstacle in spontaneous sexual reproduction of H. miconioides, so its reproduction mechanism, for example, self pollination, low seeding rate and long dormancy, needs to be thoroughly researched. The solution of these problems would be greatly significant for its conservation.

H. miconioides mainly utilizes the clone to maintain recruitment of its populations, so the clone reproduction will have a significant influence. So far, researches on clone reproduction haven't been attempted but the analysis of population structure at ramet level in Dapan Mountain (Li et al., 2004). For the future we should research the effect of clone reproduction on the genetic diversity, diameter structure and adaptive ability of H. miconioides.

Some populations of H. miconioides in the field have been undergone in different degrees by human disturbance. The habitat change perhaps has resulted in displacement of some ecological requirements. So the effect of human disturbance on H. miconioides, for example variation in its breeding system, genetic erosion, should be studied.