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C amellia changii (Family Theaceae) is a plant endemic to southern China (Zhang, Reference Zhang1999). It is known among Chinese botanists as the so-called giant panda of the plant kingdom because of its rarity and charm (Wang & Xie, Reference Wang and Xie2001). It is evergreen and grows to 4 m in height as a tall shrub or small tree (Supplementary Plate S1), and generally flowers from mid May until February. Its unusually long flowering period, large flowers and evergreen foliage make it an excellent ornamental plant and a valuable economic species (Li et al., Reference Li, Cui, Zheng, Luo and Zhou2004). Nevertheless, C. changii is not commonly grown. The objectives of the study reported here were to investigate the current status of the sole wild C. changii population and its habitat, explore the causes of its rarity, analyse the need for the protection of C. changii and recommend conservation measures.
We examined all specimens of C. changii deposited in the herbaria of the South China Botanical Garden (Chinese Academy of Sciences, SCBI) and Sun Yat-sen University (SYS). Both herbaria are major depositories for collections of plant material from southern China. In addition we used the Flora of China (Zhang, Reference Zhang1999), the Flora of Guangdong (Wu, Reference Wu1998) and other publications that contain information about C. changii. These sources indicated that all plants were located within Ehuangzhang Nature Reserve (Fig. 1) in Yangchun County, Yangjiang City, in south-west Guangdong Province. We then surveyed for C. changii in the Reserve from January 2009 to January 2013. The locations of all C. changii found were recorded with a global positioning system and mapped, and we recorded the elevation, slope, aspect and soil type at all locations. We established three transects (5 × 200 m) across the species’ range, which was along a stream, the Erchahe, in December 2011. For all plant species within each transect the identity, height, diameter at breast height (for trees), crown size (for shrubs and herbs), and number of plants were recorded. The leaf-area index (a dimensionless quantity that characterizes plant canopies, defined as the one-sided green leaf area per unit ground surface area) was measured with an LAI-2000 plant canopy analyser (LI-COR, Biosciences, Lincoln, USA). At each transect, we selected three arbitrary points, along the slope, at which five leaf-area index measurements were taken from different directions. In December 2012 soil samples were collected from three arbitrarily selected points in each transect, using a 5 cm diameter soil corer, to a depth of 20 cm. The soil samples were air dried and sieved for analysis of physical and chemical characteristics. We chose five mature individuals of C. changii for observation of sexual reproduction from January 2009 to January 2013. The number of flowers, fruit, seeds and seedlings per individual were recorded.
Fig. 1 The range (rectangle) of Camellia changii on the banks of a stream, the Erchahe, in Ehuangzhang Nature Reserve. The black dot indicates the location of the administration building in the Reserve. The inset indicates the location of the main figure in Guangdong province in southern China.
The C. changii population occupies an area 8–10 m wide and 4 km long, on both banks of the Erchahe. Altitude is 50–150 m, and slopes are 5–12°, with easterly and westerly aspects along the water catchment (Fig. 1). We found a total of 1,039 individuals of C. changii, fewer than the number (1,200) estimated by Zhang & Liang (Reference Zhang and Liang2003). About 84% of the individuals were taller than 3 m. There were no seedlings and few small plants (height < 0.5 m).
A total of 160 vascular plant species were recorded in the three transects (Supplementary Table S1). The plant community is a secondary tropical evergreen broadleaved forest (Luo et al., Reference Luo, Mo, Tang, Zheng, Huang, Zhuang and Huang2008), dominated by species of Camellia and of the families Rubiaceae and Lauraceae. The canopy is not continuous, with 48% canopy cover and a mean leaf-area index of 1.92 ± SE 0.10. Individuals of C. changii are scattered in the Gordonia axillaries–Ormosia emarginata–Syzygium buxifolium–Dicranopteris pedata community in exposed locations. The associated soil is well-drained, acidic, sandy loam with low contents of water, phosphorus and organic matter but high contents of potassium (Supplementary Tables S2–3). This combination of soil properties is atypical for this region.
Individual C. changii produced a mean of 381 ± SE 135 flowers per year (n = 5 plants) but only 5 ± SE 1 fruits and 3 ± SE 2 seeds per fruit. The dominance of medium-sized to large plants and the absence of seedlings indicate that the population is declining. The observed low rate of fruit production may be the result of a combination of factors. Fruit set in C. changii relies on insect pollinators but the species is self-incompatible and exhibits heterostyly, which, coupled with low pollinator visitation frequencies, are responsible for a high abortion rate (Luo et al., Reference Luo, Tang, Mo and Zhuang2011). The low rate of seed production we observed and the poor seed quality and low seed germination rate observed in other studies (Xue et al., Reference Xue, Zhao, Zhang and Chen2011) presumably limit the regeneration of the species.
Considering the small size of the population, skewed population structure, low level of regeneration, very narrow geographical range and small area of occupancy, C. changii should be categorized as Critically Endangered, based on criteria B1ab(v)+2ab(v) (IUCN, 2001). Because of its desirable horticultural traits, wild individuals of C. changii have been poached aggressively by local people over the past 2 decades (authors, pers. obs.). Although poaching pressure persists the remaining plants and their habitat have been more effectively protected since the establishment of the Ehuangzhang Nature Reserve in 2000 (Luo et al., Reference Luo, Tang, Mo and Zhuang2011), with weekly monitoring by Reserve staff.
Horticultural propagation techniques, including grafting C. changii scions to rootstock of Camellia gauchowensis, Camellia oleifera and Camellia japonica, and propagation by cuttings, have been developed by private nurseries (Zhang & Liang, Reference Zhang and Liang2003; Li et al., Reference Li, Cui, Zheng, Luo and Zhou2004). The Nature Reserve took advantage of these techniques to purchase and redistribute 10,000 grafted plants to local people in 2010–2011, to support livelihoods and reduce poaching pressure.
We recommend that an integrated conservation plan is required for C. changii. As part of this plan, the Nature Reserve should continue the promotion of the established propagation techniques, using scions and cuttings from existing ex situ private and government collections, for commercial horticultural use. This measure, together with the public education and awareness programmes that are already underway, will alleviate the threats to C. changii from development of local tourism and recreation areas within the Nature Reserve, the construction of small dams, and small-holder farming. Other threats to C. changii are its restricted range, limited recruitment, and potential inbreeding depression as a result of the small population size and low genetic diversity (Luo et al., Reference Luo, Zhuang and Yang2007). As a precaution we have successfully established an ex situ collection in the experimental area of the Nature Reserve, duplicating all 1,039 wild plants by grafting two or three 2–3 cm cuttings per plant onto C. oleifera rootstock. We also recommend that artificial pollination be used to increase fruit set both in situ and ex situ, and that reintroduction should be implemented to augment the population at carefully selected locations, guided by IUCN/SSC (2013). In addition, we recommend that the species be added to the list of species with extremely small populations, which is an endangered category for plant species recognized by the State Forestry Administration of China. The placement of C. changii in this category would facilitate funding for implementation of the conservation measures we recommend.
Narrow endemic species are an important but vulnerable component of global biological diversity (Fenu et al., Reference Fenu, Mattana and Bacchetta2012; Ren et al., Reference Ren, Zeng, Li, Zhang, Yang and Wang2012). In depth analyses of the challenges to and strategies for conserving narrow endemic species such as C. changii and others (Fenu et al., Reference Fenu, Mattana and Bacchetta2011, Reference Fenu, Mattana and Bacchetta2012; Martinell et al., Reference Martinell, Pujol, Blanche, Molero and Şaez2011; Cogoni et al., Reference Cogoni, Fenu, Concas and Bacchetta2013) are needed to prevent extinction of these unique species.
Acknowledgements
This research was supported by the National Basic Research Program of China (2009CB421101) and the Guangdong Sci-Tech Planning Project (2011B060400003, 2012B060400013). We thank Qingyun Laing, Xipo Lin, Lianlian Yuan and Songjun Zeng for assistance in the field, Huilan Zhang for soil analysis, HuaguYe for species identification, Mike Maunder for comments, Bruce Jaffee for help with English, and two anonymous reviewers for their valuable comments.
Biographical sketches
Hai Ren is interested in vegetation restoration and reintroduction of rare and threatened plant species. Shuguang Jian's research interests include community ecology and the biogeography of rare and threatened plants. Yongju Chen is in charge of in situ conservation and the nursery at Ehuangzhang Nature Reserve. Hong Liu has been carrying out research on biodiversity conservation in the USA and China for the past 15 years. Qianmei Zhang is a data analyst with interests in long-term ecological studies. Nan Liu focuses on plant ecophysiology and soil monitoring. Yi Xu is interested in mapping and spatial analysis. Jian Luo conducts field monitoring and plant grafting.
