Climate change may threaten habitat suitability of threatened plant species within Chinese nature reserves

Introduction

Climate change is predicted to become a major threat to biodiversity in the 21st century, forcing plant species distributions to shift or decrease dramatically (Thuiller et al., 2005; Bellard et al., 2012; Corlett & Westcott, 2013). When the suitable habitats of plant species shift outside of the range to which plant species are adapted, these plant species face an increased risk of extinction (Thuiller et al., 2005; Summers et al., 2012). Extinction risk evaluations have been completed for woody plant species, projecting declines of many species ranges under climate change (Zhang et al., 2014). Nature reserves play an important role in the conservation of threatened plant species worldwide (Hansen et al., 1991; Xu & Melick, 2007). The establishment of nature reserves is one of the most effective methods available for conserving plant habitats and slowing plant species population declines (Saetersdal, Line & Birks, 1993; Araújo et al., 2011; Ma et al., 2013). However, climate change may affect the ability of nature reserves to protect threatened plant species and even cause extinctions of threatened plant species protected within nature reserves (Araújo et al., 2004; Araújo et al., 2011). Climate change has already been shown to endanger plant diversity in European conservation areas (Thuiller et al., 2005; Araújo et al., 2011). The ability of nature reserves to protect threatened tree plants in northeastern China under climate change was recently assessed using projected changes in species distributions (Yu et al., 2014). As plant species are already vulnerable to extinction within nature reserves, assessing the effects of continued climate change on plant distributions is essential. Specifically, climate change assessments must be integrated into the conservation management plans for threatened plant species in nature reserves based on the effects of climate change on the distributions of plant species and habitat suitability (Groves et al., 2012; Lawson et al., 2012; Fordham et al., 2013).

Recent research has evaluated the effect of climate change on threatened plant species in nature reserves using ecological niche models (ENMs; Yu et al., 2014; Wan et al., 2014; Wang et al., 2015). ENMs are a popular tool used to model climate suitability or potential distributions of plant species based on species occurrence data and environmental variables across current species ranges (Elith et al., 2011; Merow, Smith & Silander, 2013). The changes in species distributions that can be inferred with ENMs, such as future projections based on climate change, are an important tool for extinction assessment of threatened plant species (Araújo et al., 2011; Fordham et al., 2012). However, there are many challenges in applying ENMs to the conservation of plant species. Plants have limited seed dispersal and migration distances, hindering large-scale movement that might be necessary for species to survive climate change (McConkey et al., 2012, Corlett & Westcott, 2013; Iverson & McKenzie, 2013). Hence, ENMs can underestimate or overestimate future plant species distributions based on future climatic suitability as estimated by ENMs (Iverson & McKenzie, 2013; Zhang et al., 2014). Thus, we may not be able to determine effective conservation plans for threatened plant species in nature reserves under climate change in this way, which undermines the apparent usefulness of ENM assessments for threatened plant species (Hijmans & Graham, 2006; Aranda & Lobo, 2011; Pineda & Lobo, 2012). To improve the usefulness of ENMs in conservation management, we evaluated changes in habitat suitability for threatened plant species based on the current occurrences of plant populations rather than potential suitable habitats estimated from ENMs (Pineda & Lobo, 2012).

China contains rich plant diversity, including more than 10% of the world's vascular plant species owing to its large area (9.6 million km²) and high environmental heterogeneity, which encompasses boreal, temperate, subtropical, and tropical biomes (Liu & Diamond, 2005; Ren et al., 2007; Yang, Ma & Kreft, 2014). Furthermore, China harbors more threatened plant species than many other regions worldwide (Liu & Diamond, 2005; Wu et al., 2011). However, Chinese nature reserves only cover 27.5% of threatened plant species distributions (Zhang et al., 2015). Moreover, climate change poses a considerable threat to plant species in China (Wang et al., 2015).

Here, we examined the effects of climate change on threatened plant species within nature reserves by assessing changes in climate suitability based on occurrence localities of species compiled from previous field work. In this study, we used Maxent modelling to project the distributions of 82 threatened Chinese plant species from four plant types and distributed among 168 nature reserves. To accomplish this, we fulfilled two goals: (1) the assessment of changes in climate suitability ranges for threatened plants in the future and (2) the evaluation of the overlap between current and future climate suitability ranges. Finally, we suggest several effective approaches for the conservation of threatened plants in the context of climate change.

Methods

Results

For all 82 threatened plant species across 168 nature reserves, model performance assessed using AUC scores was high (all models had AUC values over 0.7; Table S1). There were significant relationships between PI values and PC estimates from Maxent modelling (Fig. S1; P < 0.001) indicating that the variables selected by a jackknife test typically have consistent and high PC and PI values for tree, shrub, herb, and fern species. The largest effect on habitat suitability for trees (PI, 24.27; PC, 41%), herbs (PI, 22.52; PC, 25%), and ferns (PI, 19.32; PC, 38%) was produced by annual mean temperature changes, and precipitation seasonality most strongly impacted the habitat suitability of shrubs (PI, 17.21; PC, 33%; Table 1). For non-climatic variables, we found that soil pH was the important variable influencing habitat suitability for shrubs (PI, 16.65; PC, 50%) and ferns (PI, 16.82; PC, 25%). Specifically, the most important variables determined in this study were annual mean temperature for Malania oleifera (a tree; PI, 95.615), precipitation seasonality for Platycrater arguta (a shrub; PI, 88.711), and soil pH for Alsophila gigantea (a fern; PI, 90.218; Table S4). In addition, we found that temperature seasonality strongly affects habitat suitability for Magnolia wilsonii (a shrub; PI, 92.327) and that mean diurnal range has an important impact on habitat suitability for Fokienia hodginsii (a tree; PI, 61.271; Table S4).

For each threatened plant species across all nature reserves, there were significantly positive relationships between C (the change in climate suitability between current and future conditions) and D (the overlap between current and future climate suitability) under the low, medium, and high greenhouse gas concentration scenarios (P < 0.001; Fig. 1). For all threatened plant species belonging to each nature reserve with a decreasing C value, D values also decreased significantly (P < 0.001; Fig. 2). Thus, we focused on C because of these significantly positive relationships between C and D under the low and high greenhouse gas concentration scenarios (Figs. 1 and 2). Climate suitability is projected to decrease significantly from low to high concentration scenarios across the different plant type groups across all the nature reserves (P < 0.001; Fig. 3) and across all threatened plant species occurring within each nature reserve independently (P < 0.001). Furthermore, C values were projected to be larger in the 2080s than the 2050s in the medium and high concentration scenarios based plant type groups (P < 0.001; Fig. 3). Moreover, C increases significantly from low to high concentration scenarios (P < 0.001; Fig. 3). Habitat suitability for tree species would decrease most severely, and climate change may have the smallest impact on fern species across all the concentration scenarios (Fig. 3). The climate suitability of 63, 65, and 65 threatened plant species are projected to decrease in the low, medium, and high concentration scenarios, respectively, by both the 2050s and 2080s (Fig. 4A; Table S5). Thuja koraiensis is projected to have the largest decrease in climatically suitable habitat under the high concentration scenario by the 2080s (Table S5).

The regions with large changes in climate suitability during the current time period are distributed across central and southern China (Fig. S2). With increasing greenhouse gas concentrations, the habitat suitability for threatened plant species in nature reserves will decrease gradually (Figs. 4B and 5). The climate suitability of 132, 140, and 151 nature reserves are projected to decrease under the low, medium and high concentration scenarios, respectively, by both the 2050s and 2080s (Fig. 4B; Table S6). Furthermore, the number of nature reserves exhibiting decreased habitat suitability for threatened plant species was larger under the medium and high concentration scenarios for the 2050s relative to the 2080s (Figs. 4B and 5). We focused on the habitat suitability of threatened plant species in nature reserves under the high concentration scenario. The nature reserves with decreasing habitat suitability of threatened plant species were distributed across Henan, Shaanxi, Sichuan, Chongqing, Guizhou, Yunnan, Guangxi, Fujian, Jiangxi, and Anhui provinces (Fig. 5). Wudaoxia nature reserve (Hubei province) exhibited the largest decrease in climate suitability under the low concentration scenario (in the 2050s), the medium concentration scenario (in the 2080s), and the high concentration scenario (in the 2080s; Table S6).

Discussion

We evaluated the climate suitability of threatened plant species in Chinese nature reserves under future climate change scenarios using occurrence locality data. We project that the habitat suitability of more than 60 threatened plants within more than 130 nature reserves would decrease under these projected climate change scenarios. Overall, this indicates that climate change may threaten habitat suitability of threatened plant species within Chinese nature reserves.

Annual mean temperature is projected to affect the habitat suitability of threatened tree, herb, and fern species most, while precipitation seasonality is the driving factor in changing habitat suitability for threatened shrub species. This indicates the importance of monitoring threatened plant species according to factors such as plant type. This is consistent with previous studies that found that annual mean temperature was the most important bioclimatic variable for the distribution and growth of trees, herbs, and ferns (Zhang et al., 2014; Yu et al., 2014; Wang et al., 2015). The annual mean temperature is projected to increase dramatically in the 2080s. Hence, annual mean temperature may dramatically alter the distribution of plant species. Dilts et al. (2015) showed that the water balance influenced by precipitation seasonality is related to the geographic distribution of most shrub species. By the 2080s, precipitation seasonality may also change substantially with increasing greenhouse gas concentrations. Hence, we also focused on the role of precipitation seasonality on habitat suitability or threatened plant species. Moreover, the impact of soil pH on habitat suitability for tree, shrub, and fern species was substantial (Ervin & Holly, 2011; Marschner, Crowley & Yang, 2004). Soil pH affects nutrient availability, which dramatically impacts habitat suitability (Ervin & Holly, 2011; Marschner, Crowley & Yang, 2004). To address the practical conservation issues, we must consider the impact of future climate change coupled with factors such as soil pH on habitat suitability for threatened plant species, particularly, tree, shrub, and fern species.

Based on the Global Strategy for Plant Conservation (http://www.cbd.int/gspc/), at least 75% of known threatened plant species are protected. Projected climate changes caused by high greenhouse gas emissions are projected to damage suitable habitats for plant species within Chinese nature reserves. The large shift in potential habitat distributions and decreases in habitats with suitable climates could leave potentially viable populations of threatened plant species vulnerable to extinction (Fordham et al., 2013; Costion et al., 2015; Van Andel et al., 2015). Hence, we compiled a list of important plants for conservation within China including more than 60 threatened plant species (over 73.2% of all 82 species), for example, T. koraiensis, which is particularly endangered by trends of climate suitability under the high concentration scenario. In particular, extreme climate events and rapid changes in climate can cause physiological stress and damage to plants (Bastos et al., 2014; Zinta et al., 2014). Threatened plant species are already in danger and thus are vulnerable to extreme climate events like the 2003 summer heatwave, showing that inappropriate land management can threaten the existence of plant species (Bastos et al., 2014; Zinta et al., 2014; Wujeska-Klause, Bossinger & Tausz, 2015). Furthermore, we found that the threatened tree species within nature reserves would be strongly affected by climate change, particularly under the high concentration scenario by the 2080s. The distributions of suitable habitats for tree species may shift as a consequence of climate change. Alberto et al. (2013) has shown that evolutionary responses are required for tree populations to track climate change. Hence, we must assess the impact of climate change on habitat suitability for tree species when managing the conservation of threatened plant species. Although fern species may be affected less by climate change, we still must pay attention to the response of fern species like Alsophila denticulate, Cibotium barometz, and Alsophila metteniana because their suitable habitats decrease substantially under the high concentration scenario. Hence, we must monitor the changing dynamics of potential distributions of threatened plants under climate change and prevent habitat degeneration in order to stabilize plant populations (Thuiller et al., 2005; Keith et al., 2008; Araújo et al., 2011).

Furthermore, many threatened species are valued for their economic potential and medicinal properties (Wang et al., 2015). For example, the important anticancer drug camptothecin is extracted from Camptotheca acuminata (Kusari, Zühlke & Spiteller, 2009). However, the habitat of viable populations of C. acuminata has decreased as a result of environmental pollution, deforestation, and erosion (Yu et al., 2014; Wang et al., 2015). Moreover, climate change may aggravate the already stressed remnant populations of C. acuminata (Table S1). The value of wild plant resources may be diminished by climate change. Previous studies have also shown that plant species may need to escape to higher latitudes and altitudes to evade rising temperatures (Thuiller et al., 2011). Furthermore, threatened plant species with narrow climate niches would be threatened severely by climate change (Ma et al., 2013). Our results, in combination with those of previous studies, highlight the need for monitoring and managing threatened species under projected decreasing climate suitability as well as the value of determining congruence between current and future climatically suitable habitats (Thuiller et al., 2011; Fiedler, 2012; Costion et al., 2015).

Climate change threatens habitat suitability for threatened plant species in more than 130 nature reserves (77.4% of all the nature reserves in the analysis) under the low greenhouse gas concentration scenario, 140 reserves under the medium concentration scenario (83.3%), and 165 reserves (98.2%) under the high concentration scenario by both the 2050s and 2080s. This indicates that climate change will likely decrease the capacity of these nature reserves to protect threatened plants. These nature reserves play an important role in ecosystem services (Xu & Melick, 2007; Araújo et al., 2011; Yu et al., 2014). For example, Ailaoshan nature reserve exhibits rich plant diversity and stores a large quantity of carbon (Qiao et al., 2014). However, climate change will alter the habitat suitability for many threatened plant species in this nature reserve, possibly disrupting ecosystem services such as carbon storage (Heller & Zavaleta, 2009). Hence, we must take effective measures to reduce the negative effect of climate change on threatened plants within nature reserves, particularly Wudaoxia nature reserve as it is projected to suffer most severely in term of decreasing habitat suitability for threatened plant species.

Conclusions

Our method serves as an important reference for the conservation of plant diversity in the face of climate change. This goal will require both increased research and a continually developed capacity to forecast future climate conditions, as well as identification of the responses of threatened plant species to climate change. An integrative assessment of climate suitability using occurrence localities will enhance the conservation status system for threatened plant species. As climatically suitable habitats decrease for threatened plant species, niche gaps may increase in the future. Climate change may threaten habitat suitability for more than 60 threatened plant species within Chinese nature reserves across more than 130 nature reserves. Hence, climate change is likely to threaten habitat suitability for threatened plant species throughout Chinese nature reserves. Future studies should consider more local scales when making assessments of conservation status for threatened plant species. We urgently need innovative evaluation approaches for threatened plant species at all scales.

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