The concept of Plant Species with Extremely Small Populations (PSESP) has been employed to guide conservation of threatened plant species in China. Climate change has a high potential to threaten PSESP. As a result, it is necessary to integrate climate change effects on PSESP into conservation planning in China. Here, ecological niche modelling is used to project current and future habitat distributions of six PSESP in China under climate change scenarios and conservation planning software is applied to identify priority conservation areas (PCAs) for these PSESP based on habitat distributions. These results were used to provide proposals for in-situ and ex-situ conservation measures directed at PSESP. It was found that annual precipitation was important for habitat distributions for all six PSESP (with the percentage contribution to habitat distributions ranging from 18.1 % to 74.9 %) and non-climatic variables including soil and altitude have a large effect on habitat suitability of PSESP. Large quantities of PCAs occurred within some provincial regions for these six PSESP (e.g. Sichuan and Jilin for the PSESPCathaya argyrophylla, Taxus cuspidata, Annamocarya sinensis and Madhuca pasquieri), indicating that these are likely to be appropriate areas for in-situ and ex-situ conservation measures directed at these PSESP. Those nature reserves with large quantities of PCAs were identified as promising sites for in-situ conservation measures of PSESP; such reserves include Yangzie and Dongdongtinghu for C. argyrophylla, Songhuajiangsanhu and Changbaishan for T. cuspidata and Shiwandashanshuiyuanlian for Tsoongiodendron odorum. These results suggest that existing seed banks and botanical gardens occurring within identified PCAs should allocate more resources and space to ex-situ conservation of PSESP. In addition, there should be additional botanical gardens established for ex-situ conservation of PSESP in PCAs outside existing nature reserves. To address the risk of negative effects of climate change on PSESP, it is necessary to integrate in-situ and ex-situ conservation as well as climate change monitoring in PSESP conservation planning.

PSESP, climatic change, systematic conservation planning, China, in-situ and ex-situ conservation measures

Climate change has a large potential to threaten plant diversity from species to biomes, as well as hinder endangered species protection (Thuiller et al. 2005, Bellard et al. 2012, Diez et al. 2012, Grimm et al. 2013, Watson et al. 2013). Climate change may result in the migration, vulnerability or extinction of plant species by causing species distributions to shift, habitat fragmentation to increase, population sizes to decrease and genetic diversity to decline (Thuiller et al. 2005, Heller and Zavaleta 2009, Bellard et al. 2012, Diez et al. 2012, Grimm et al. 2013, Watson et al. 2013). Furthermore, other human impacts are likely to cause additional habitat loss and threaten plant species (Tilman and Lehman 2001, Kier et al. 2005, Vásquez et al. 2015). In particular, threatened plants with narrow niche width and small population sizes may fail to adapt to novel climatic conditions and thus become endangered or even extinct (Bellard et al. 2012, Botts et al. 2013, Slatyer et al. 2013). Future climate may change rapidly and enhance loss of threatened plant species stemming from vulnerability to climate change, which is influenced by species’ sensitivity and adaptive capacity, as well as the degree of exposure (Thuiller et al. 2005, Bellard et al. 2012, Diez et al. 2012, Watson et al. 2013). Plant conservation faces great uncertainty as a result of climate change; decreasing this uncertainty is a challenge for conservation biologists and government managers (Lavergne et al. 2004, Heller and Zavaleta 2009). There is a need to integrate climate change into conservation planning for threatened plants.

As many of its species are currently threatened or on the brink of extinction, China is one of the highest priorities for biodiversity conservation globally (López-Pujol et al. 2006, Wang et al. 2015, Zhang et al. 2015, Feng et al. 2017). It is urgent for China to take effective measures to conserve threatened plant species. A list of 120 wild plant species was recently identified as the first set of species in the nation to receive urgent protection (Ren et al. 2012, Volis 2016). These 120 species are labelled Plant Species with Extremely Small Populations (PSESP) due to: 1) the limited number of mature individuals in the wild; 2) restricted distribution ranges; 3) recognition as national or regional endemic species in China; and 4) economic development or scientific value (Ma et al. 2013, Chen et al. 2014, Wade et al. 2016, Volis 2016, Wang et al. 2017). To conserve the 120 PSESP, several national and regional conservation strategies have been implemented and such strategies will be expanded across China (Ren et al. 2012, Ma et al. 2013). In-situ and ex-situ conservation methods have been widely employed for PSESP (Ren et al. 2012, Ma et al. 2013, Wade et al. 2016, Volis 2016). These approaches have the advantage of being cost-efficient, flexible and capable of supplementing other conservation measures (Wade et al. 2016, Volis 2016). However, due to the vulnerability of PSESP to rapid climate change, the effectiveness of in-situ and ex-situ PSESP conservation actions may be decreased by climate change (Chen et al. 2014, Wang et al. 2017). Planning long-term in-situ and ex-situ conservation strategies for the protection of PSESP under scenarios of climate change can be challenging (Wang et al. 2017).

Identifying priority conservation areas (PCAs) is a useful step in making climate change adaptation strategies for the conservation of PSESP. Recently, many conservation biologists and ecologists have used ecological niche modelling (ENM) in combination with conservation planning software to identify PCAs for endemic, threatened and endangered plant species under climate change conditions (Pérez and Font 2012, Wan et al. 2014, 2015, Adams-Hosking et al. 2015, Wang et al. 2015). ENMs, which are based on occurrence records and climatic variables, are widely used to predict spatial distribution patterns of species diversity (Merow et al. 2013, Adams-Hosking et al. 2015, Wang et al. 2015). Such models are used to generate proposals for biological conservation actions and to examine their probable feasibility (Adams-Hosking et al. 2015, Wang et al. 2015, Abrahms et al. 2017, Reside et al. 2017). For example, ENMs may enable conservation practitioners to predict previously unknown locations of species (Pearson et al. 2007). Conservation planning software is commonly used to generate a spatial conservation framework that can be used to prioritise large-scale conservation projects that involve numerous species or to identify the most effective conservation areas that will capture target species, as predicted by the results of ENMs (Moilanen 2007, Di Minin and Moilanen 2012, Lehtomäki and Moilanen 2013, Wan et al. 2014, Abrahms et al. 2017). The ability of existing or proposed nature reserves to protect threatened plants can be evaluated using ENMs and conservation planning software and new conservation areas could be designated in order to respond to climate change effects (Wan et al. 2014, 2015, 2017, Wang et al. 2016). In this way, the plant conservation effectiveness of a network of nature reserves can be maximised under climate change conditions (Wan et al. 2015, Wang et al. 2016, Abrahms et al. 2017). For example, Wang et al. (2015) used ENM coupled with conservation planning software to identify PCAs for threatened plants in China under climate change. The habitat distributions of PSESP are related to the climatic variables temperature and precipitation and therefore may be affected negatively by future climate change (Wang et al. 2017). Hence, there is a need to identify PCAs for PSESP in China under climate change conditions and to provide a simple protection assessment system for either in-situ or ex-situ conservation measures.

PSESP as a designation is not only important for conservation prioritisation in China, but also may be a useful framework in conservation efforts for threatened plants around the world (Wang et al. 2017). As a consequence of climate change, species will respond by shifting their distributional ranges and some populations may shrink to the point of extinction (Thuiller et al. 2005, Mawdsley et al. 2009, Bellard et al. 2012, Grimm et al. 2013, Watson et al. 2013). Hence, it is important for conservation biologists and governmental managers to integrate the impacts of climate change on habitat distributions of plants into conservation planning for PSESP (Mawdsley et al. 2009, Bellard et al. 2012). Here, PCAs are delineated and potential sites identified for conservation of PSESP in China under climate change conditions (Chen et al. 2014, Wade et al. 2016, Volis 2016, Wang et al. 2017). Conservation of PSESP in China requires an integrated approach, encompassing both in-situ and ex-situ conservation measures and their methodologies, as well as establishing effective evaluation systems for PSESP (Wade et al. 2016, Volis 2016, Wang et al. 2017). In-situ conservation measures, which may occur within nature reserves and other types of scenic locations, can be used to maintain the evolutionary and biological reproductive potential of the ecological system (Wade et al. 2016, Volis 2016). Ex-situ conservation measures, in which parts of the population are placed in a new location, can be used to identify suitable living environments for species for the future and to retain existing populations (Wade et al. 2016, Volis 2016). By definition, PSESP have a limited number of individuals and small population sizes in China (Wade et al. 2016, Volis 2016). Natural regeneration of PSESP is poor and some species have no chance of survival (Ren et al. 2012, Ma et al. 2013). There is a need for increased research on reproduction, wild endangered population dynamics, conditions conducive to growth and seed bank establishment to facilitate ex-situ conservation of PSESP (Wade et al. 2016, Volis 2016).

The primary objective of this study is to identify PCAs for PSESP in China under climate change conditions. To achieve this objective, six PSESP were selected as study species and ENM used to model the habitat distributions of these PSESP under current and future climate scenarios and the environmental variables that contribute significantly to the habitat distributions of the focal PSESP were explored. Then, conservation planning software was used to identify PCAs for PSESP in China under projected climate change conditions based on the species’ habitat requirements. Finally, the regions were identified with high potential to serve as effective conservation sites for the focal PSESP based on identified PCAs and suggestions were developed for in-situ and ex-situ conservation measures of PSESP.

All ENMs had AUC values greater than 0.7 for both the training and test data sets and the training omission rates were less than 17 %, indicating a high level of accuracy for each model (Table 1). Annual precipitation was important for the distributions of all six PSESP (with PCs ranging from 18.1 % to 74.9 %; Table 2). The annual precipitation response curves of distributions of T. cuspidata, A. sinensis and T. odorum were single peak in shape (Fig. 2b, c, e). Response curves indicated that with increasing annual precipitation, habitat suitability of C. argyrophylla, U. elongata and M. pasquieri is likely to increase and then remain stable (Fig. 2a, d and f). Temperature seasonality contributes substantially to the distribution of T. cuspidata and precipitation seasonality was the most important variable influencing distributions of C. argyrophylla and U. elongata (Table 2). Soil variables, such as bulk density, cation exchange capacity and sand as a fraction of soil texture, exert a large effect on distributions of C. argyrophylla, T. cuspidata and U. elongata. Habitat suitability of A. sinensis was affected by altitude (PC = 18.4%; Table 2).

Figure 2.

Response curves of annual precipitation to habitat suitability for six PSESP.

Out of all provinces, the greatest total area of PCAs for the studied PSESP occurred in Sichuan and Jilin; PCAs in these provinces included those of C. argyrophylla, A. sinensis and M. pasquieri and T. cuspidata (Fig. 3). Overall, PCAs of C. argyrophylla occurred in Anhui, Henan, Hubei, Hunan, Jiangsu and Jiangxi (Fig. 3). For T. cuspidata, PCAs occurred in Heilongjiang, Jilin and Liaoning; PCAs for A. sinensis occurred in Sichuan, Hubei, Shaanxi and Tibet; PCAs for U. elongata occurred in Jiangxi, Fujian and Hunan; PCAs of T. odorum occurred in Guangdong and Guangxi; and PCAs for M. pasquieri occurred in Sichuan, Tibet and Jiangxi (Fig. 3).

Figure 3.

Priority conservation areas for six PSESP in China under climate change.

The nature reserves with largest capacity to conserve the focal PSESP included Yangzie, Songhuajiangsanhu, Changbaishan, Dongdongtinghu and Shiwandashanshuiyuanlian (Figs 1, 3; Suppl. material 1: Table S2). Specifically, PCAs indicate that Yangzie and Dongdongtinghu are highly suitable for C. argyrophylla and Songhuajiangsanhu and Changbaishan demonstrate high PCA occurrence for T. cuspidata (Figs 1, 3; Suppl. material 1: Table S2). There is high overlap between PCAs of A. sinensis and the existing nature reserves Baishuijiang and Cuiyunlanggubai, between PCAs of U. elongata and the reserves Jiangxiwuyishan and Mountwuyi, between PCAs of T. odorum and the reserves Shiwandashanshuiyuanlian and Xishuangbanna and between PCAs of M. pasquieri and the reserves Cuiyunlanggubai and Jinyunshan (Figs 1, 3; Suppl. material 1: Table S2).

These results indicate that some provincial regions (e.g. Sichuan and Jilin) contain large areas of habitat as identified by the PCAs for the six PSESP. As such, the outputs serve as tools to identify potential areas for the conservation of PSESP. Figure 3 may be regarded as an important reference for determining promising locations for in-situ and ex-situ conservation efforts directed at PSESP. In-situ and ex-situ conservation are effective approaches for protecting PSESP (Wade et al. 2016, Volis 2016, Wang et al. 2017). Via in-situ conservation, protection in each region is increased, establishing local protected zones for PSESP that conserve the natural environment. In China, many nature reserves have been established for conservation of threatened plant species (Wade et al. 2016, Volis 2016). For example, the aim of the nature reserves in Muling was to protect T. cuspidata. Based on these results, it is suggested that the Songhuajiangsanhu and Changbaishan nature reserves also have high potential to be effectively used for conservation actions for T. cuspidata. Furthermore, Yangzie and Shiwandashanshuiyuanlian have the potential to play an important role in the protection of C. argyrophylla. This study identifies key existing nature reserves for in-situ conservation of C. argyrophylla, T. cuspidata, A. sinensis, U. elongata, T. odorum and M. pasquieri. Within these reserves, the construction of small nature reserves, eco-orchards and forest eco-stations for in-situ conservation should be bolstered (Wade et al. 2016, Volis 2016). However, climate factors, including temperature and precipitation, should be regarded as important monitoring indicators for in-situ conservation of PSESP because future climate change may alter suitable sites for PSESP (Suppl. material 1: Figure S1). Just as existing habitats are predicted to be disrupted by climate change, in some cases forcing the use of ex-situ conservation, newly established conservation sites may be impacted in the future (Wang et al. 2017).

In an attempt to take into account these future scenarios, current and future suitable distributions were integrated into PCA predictions in order to consider where and how ex-situ conservation could be used in PCAs for PSESP (Wang et al. 2015). Vulnerability of PSESP to climate change must be adopted as the most important indicator that the species is really endangered due to climate change effects. As shown in Fig. 3, PCAs often included areas outside the network of established nature reserves, indicating that ex-situ conservation or the establishment of new protected areas with less vulnerability to predicted climate change may be appropriate for species currently reliant on nature reserves (Wang et al. 2016; Wan et al. 2018). For instance, Cuiyunlanggubai and Jinyunshan appear to be suitable experimental areas for future research on M. pasquieri and Baishuijiang and Cuiyunlanggubai are likely to be key nature reserves for ex-situ conservation for A. sinensis. The construction of conservation areas for PSESP should be increased in PCAs outside existing nature reserves (Wade et al. 2016, Volis 2016). For example, few seedlings have been observed in natural populations of A. sinensis and climate change has a large potential to decrease the distribution probability; thus, both range and population sizes are projected to decline for A. sinensis (Wade et al. 2016, Volis 2016). To conserve A. sinensis, it is necessary to mitigate the impacts of climate change by establishing areas of ex-situ conservation with the ability to adapt to future climate change for A. sinensis (Wade et al. 2016, Volis 2016). Existing seed banks and botanical gardens occurring within PCAs should allocate more resources and space to PSESP. Usage of integrated ex-situ/in-situ approaches must become the norm for PSESP.

It was found that climatic variables and, particularly annual precipitation, were important for distributions of the six focal PSESP in China (Table 2), indicating that there is a need to consider climate change when planning PSESP conservation efforts via in-situ and ex-situ measures. PSESP with a high protection value, such as plants with high scientific research values and ornamental plants, are threatened by over-exploitation and utilisation, habitat fragmentation and the small sizes of their wild populations in broad-leaved forests and bush fallows (Wang et al. 2017). For example, for T. odorum and M. pasquieri, habitat fragmentation is very severe in China (Wang et al. 2017). Population persistence and growth are at high risk for T. odorum and M. pasquieri. As discussed for A. sinensis, above, populations of PSESP that are already this vulnerable may be further impacted by rapid climate change (Bellard et al. 2012, Wang et al. 2016, 2017). Future climate change has a large potential to impact populations, individuals and habitats of PSESP in China. Wang et al. (2017) has shown that high temperatures and low temperature seasonality could influence the occurrence of suitable habitats for the PSESP in China. For example, these results demonstrate that temperature seasonality could affect distributions for T. cuspidata (Table 2). However, these models found different distribution responses to climatic variables for different PSESP, suggesting that different conservation strategies will be necessary for the different PSESP. The importance of each climatic factor may vary depending on the PSESP of interest (Fig. 2). There is a need to monitor the patterns of responses of habitat suitability to environmental variation for these six PSESP. However, it is also important for protection efforts to consider non-climatic factors, such as soil, vegetation types, slope, aspect and elevation etc., so that protection areas can be chosen appropriately (Parmesan et al. 2005, Schwartz et al. 2006, Austin and Van Niel 2011, Oke and Thompson 2015). Altitude and soil variables, including bulk density, cation exchange capacity and fraction of sand as a component of soil texture, have a large contribution to distributions of PSESP (Table 2).

To address the negative effects of climate change on PSESP, there is a need to integrate in-situ and ex-situ conservation measures and climate change monitoring into conservation planning for the six focal PSESP. The delineation of PCAs may be used for providing in-situ and ex-situ conservation measures for PSESP populations and habitats. Monitoring of environmental variation is essential for successful in-situ and ex-situ conservation management of PSESP (Wade et al. 2016, Volis 2016; Wan et al. 2018). However, limits to this study include a need for more detailed empirical data collection. Future studies must take future land use and land cover into account in conservation planning and consider conservation management needs of more PSESP under future global change. Furthermore, PSESP as a designation is likely to be globally useful and it is recommended that global assessments of species be selected based on PSESP criteria.

We thank for the valuable comments of editor and reviewers for the improvement of the early manuscript. This work has been supported by the project entrusted by China’s State Forestry Administration “Effectiveness assessment of small nature reserves: a case of Lin’an city, Zhejiang Province”.