1. Introduction

Medicinal plants provide important ecosystem services, e.g., healthcare, local economic benefits, cultural value and heritage, especially in developing countries (Hamilton, 2004; Chen et al., 2016). An estimated 80% of the global population depends on traditional medicinal plants for their primary health care (WHO, 2002; Hamilton, 2004). In 2015, the output value of traditional medicine in China alone was about $124.9 billion (The State Council Information Office of the People's Republic of China, 2016). However, because most of these medicinal materials are collected from wild resources, many species are threatened by habitat destruction and overharvesting (Huang et al., 2012; Chen et al., 2016). Therefore, an important question in biodiversity conservation and ecosystem management is how medicinal plants are naturally distributed and which factors affect their distribution.

Numerous hypotheses have linked biodiversity distribution with contemporary climate (Currie et al., 2004; Wiens and Donoghue, 2004). One of the main explanations is that tropical regions with wet and warm climates harbor higher biodiversity by providing higher productivity, more species interactions, greater ecological specialization, more chances for speciation, and lower extinction rates (Currie et al., 2004; Wiens and Donoghue, 2004; Mittelbach et al., 2007). Previous studies on the distribution of medicinal plants also suggest the importance of contemporary climate (Kaky and Gilbert, 2016; Li et al., 2016). For example, medicinal plant ratios (defined as medicinal plant richness divided by overall vascular plant richness) in Xinjiang, China are highly correlated with contemporary precipitation and temperature (Li et al., 2016). In Egypt, temperature is the most important predictor used to build species distribution models for medicinal plants (Kaky and Gilbert, 2016).

In addition to the contemporary climate, paleoclimate change may have also significantly influenced the distribution of current biodiversity, especially that of endemic species, mainly through its effects on speciation and extinction (Sandel et al., 2011; Feng et al., 2016; 2019). For example, both Chinese endemic bird and plant species have been found to be concentrated in regions with stable glacial-interglacial climates, e.g., southwestern China (Feng et al., 2016; 2020). Notably, about 3150 of the 13, 000 traditional Chinese medicinal plant species are endemic to China (Huang and Ma, 2017). However, it is still not clear if the distribution of these endemic medicinal plant species is associated with paleoclimate change. In addition to these climate related variables and hypotheses, general species richness and endemic species are also significantly associated with environmental heterogeneity, which is usually represented by altitudinal range (Stein et al., 2014; Feng et al., 2016; 2020).

Besides these natural variables, another important driver of medicinal plant distribution is cultural diversity, e.g., indigenous knowledge and ethnic diversity (Caballero-Serrano et al., 2019; Cámara-Leret et al., 2019). The cultural diversity of diverse indigenous communities contributes greatly to medicinal plants through traditional knowledge, including the recognition and use of medicinal plants. In addition, indigenous communities with sophisticated knowledge of plants and their services also depend on these plants for both medicine and food (Cámara-Leret et al., 2019). Notably, a global study showed that cultural diversity and biological diversity always co-occur in biodiversity hotspots (Gorenflo et al., 2012). However, it is currently still unknown how the distribution of medicinal plants is affected by cultural diversity at a regional/national scale.

China has huge ethnic diversity, with 55 ethnic minorities. China also has diverse medicinal plants, especially endemic medicinal plant species (Huang and Ma, 2017). Endemic medicinal plant species are important natural resources in China that play a crucial role in the development of China's economy and society. Thus, understanding how these species are distributed and which factors affect their distributions are important questions not only for ecology and biogeography, but also for the economy and society in China (Huang and Ma, 2007). However, no studies have systematically assessed the distribution patterns of endemic medicinal plant species in China, or determined whether the distribution of endemic medicinal plant species is associated with paleoclimate change, contemporary climate, habitat heterogeneity, or cultural diversity. Here, we used the Chinese Angiosperm Plant Distribution Database and a comprehensive list of Chinese endemic medicinal plant species to 1) determine the conservation status of all Chinese endemic medicinal plant species; 2) assess the distribution patterns of Chinese endemic medicinal plant species at the prefecture city level; and 3) identify whether the distribution of endemic medicinal plant species in China is correlated with regions with stable paleoclimate, warm and wet contemporary climate, high environmental heterogeneity, or diverse ethnic groups.

2. Materials and methods 2.1. Data on Chinese endemic medicinal plant

The species list (3135 species) of Chinese endemic medicinal plant was compiled from the Endemic Species of Chinese Medicinal Plants (Huang and Ma, 2017). Distribution of these species at the prefecture city level was compiled from the Chinese Angiosperm Plant Distribution Database (including 3017 species, as 118 species were not included in this database; Lu et al., 2018). We used two recent publications to check the IUCN conservation status of all endemic medicinal plant species examined in this study (Qin et al., 2017; Yang, 2021).

2.2. Explanatory variables

Contemporary climate (average values for the years 1960–1990) was represented by mean annual temperature (MAT) and mean annual precipitation (MAP), which were downloaded from WorldClim (Hijmans et al., 2005). Glacial-interglacial climate anomaly was calculated as the contemporary MAT/MAP minus the Last Glacial Maximum MAT/MAP, which were computed as the mean of the Community Climate System Model version 3 (CCSM3; Hijmans et al., 2005; Otto-Bliesner et al., 2006) and Model for Interdisciplinary Research on Climate v.3.2 (MIROC3.2; Hasumi and Emori, 2004). Data on altitude was also downloaded from WorldClim (Hijmans et al., 2005). The values of the four climate variables (MAT, MAP, anomaly in MAT, anomaly in MAP) for each city were calculated as the mean values of these variables (the resolution is 2.5 min) in each polygon covered by each city. Altitudinal range for each city was calculated as the maximum altitude minus the minimum altitude in each city, which was used to represent environmental heterogeneity. The values of these five variables in each city were calculated using 'Zonal Statistic as Table' tool in ArcGIS 10.3. Ethnic minority population size and the overall population size of each city were collected from six national demographic censuses taken in 2010 (http://www.stats.gov.cn/ztjc/zdtjgz/zgrkpc/dlcrkpc/).

2.3. Statistics

Ratio of endemic medicinal plant species richness in each city was calculated as the endemic medicinal plant species richness divided by overall plant species richness in that city, which was also compiled from the Chinese Angiosperm Plant Distribution Database (including distribution information of 27, 005 species, Lu et al., 2018). Endemic medicinal plant species richness was logarithm transformed to get a normal distributed residual. All dependent and independent variables were standardized (standard deviation = 1 and mean = 0) to make the regression coefficients comparable.

Ordinary least squares models were used to check the associations between endemic medicinal plant species richness, ratio of endemic medicinal plant species richness and each explanatory variable. In addition, simultaneous autoregressive models were used to control the spatial autocorrelation in regression residuals. All these analyses were conducted in R version 3.6.0 (R Core Team, 2016). The packages used here were 'vegan' (Oksanen et al., 2019) and 'spdep' (Bivand et al., 2015).

3. Results

Of the 3135 endemic medicinal plant species, 345 species are threatened at different levels, including 38 critically endangered species, 102 endangered species and 205 vulnerable species. Both endemic medicinal plant species richness and the ratio of endemic medicinal plant species richness were relatively high in southern China, especially in southwestern China (Fig. 1A and B). There were four cities (Chongqing and three cities in Sichuan Province) with more than 1000 endemic medicinal plant species, and six cities (two in Hubei Province and four in Sichuan Province) with ratios of endemic medicinal plant species richness larger than 0.25. Furthermore, southern China had a relatively stable glacial-interglacial climate (especially in southwestern China) and more precipitation (Fig. 1C and D).

Ordinary least squares models and simultaneous autoregressive models showed similar patterns, i.e., both endemic medicinal plant species richness and the ratio of endemic medicinal plant species richness were negatively associated with glacial-interglacial anomaly in temperature, and positively associated with precipitation and altitudinal range (Table 1; Fig. 2). In addition, endemic medicinal plant species richness was positively associated with ethnic minority population size and the ratio of the ethnic minority population to the total human population (Table 1).

4. Discussion 4.1. Distribution of Chinese endemic medicinal plant species

Based on a comprehensive list of Chinese endemic medicinal plant species and the Chinese Angiosperm Plant Distribution Database, our results show that southern China, especially southwestern China, harbor more endemic medicinal plant species than northern China. A recent study also found hotspots of commonly used traditional Chinese medicinal plants in southern China (Shan et al., 2022). Another study found that species richness of threatened medicinal plants is also higher in southern China than in northern China, especially in Yunnan and Sichuan provinces (Chi et al., 2017). In addition, many studies have concluded that southwestern China is an important biodiversity hotspot, harboring more overall plant, animal and bird species (Tang et al., 2006; Wang et al., 2020), a higher proportion of endemic plant and endemic bird species (Lei et al., 2003; Feng et al., 2016; 2020), as well as more threatened plant and threatened bird species (Feng et al., 2017; Yang et al., 2021). Taken together with these previous findings, our results emphasize the crucial role of southwestern China in biodiversity conservation in China.

4.2. Stable climate promotes more endemic medicinal plant species

The orbitally forced species' range dynamics (ORD) hypothesis suggests that long-term glacial-interglacial climate changes, particularly the Quaternary glacial-interglacial shifts, have significantly influenced current biodiversity patterns, especially the distribution of endemic species (Dynesius and Jansson, 2000; Svenning et al., 2015). According to the ORD hypothesis, regions with a relatively stable paleoclimate may have both lower extinction rates and higher speciation rates, which may allow them to harbor more paleoendemics and neoendemics (Dynesius and Jansson, 2000). Supporting this hypothesis, previous studies in China have already found significant and negative associations between glacial-interglacial climate instability and richness of endemic plant species and endemic bird species (Feng et al., 2016; 2020). Our finding that glacial-interglacial climate stability is associated with higher numbers of endemic medicinal plant species is consistent with these studies and supports the ORD hypothesis. This finding again suggests that special attention should be paid to the conservation of historically well-preserved biodiversity in these regions, especially in the context of unprecedented global climate change.

4.3. High precipitation promotes more endemic medicinal plant species

It has been widely shown that biodiversity distribution is strongly associated with contemporary climate, with many different hypotheses linked to both temperature and precipitation (Currie et al., 2004; Wiens and Donoghue, 2004). Notably, many studies have tested associations between contemporary climate and the distribution of medicinal plant species (Li et al., 2015; 2016). Specifically, in northwest China medicinal plant ratios, defined as the value of medicinal plant richness divided by vascular plant richness, was found to be highly correlated with contemporary climate (Li et al., 2016). Another study using species distribution models found that climate variables related to contemporary temperature and precipitation can be used to predict the potential distribution of a medicinal plant (Homonoia riparia Lour) in China (Yi et al., 2016). Consistent with these studies, our results showed that contemporary precipitation was a significant and strong predictor for the distribution of endemic medicinal plant species across the whole of China. Importantly, these results suggest that the warmer and drier climate expected due to global climate change (Hui et al., 2018) will pose great challenges to the conservation of China's endemic plant species. For example, one study has shown that future climate change will significantly affect the distribution of medicinal plant species in Spain, especially that of narrow endemics (Munt et al., 2016).

4.4. Other explanatory variables

Medicinal plant species provide crucial ecosystem services to humans, especially in indigenous communities in remote areas of developing countries (Chen et al., 2016; Cámara-Leret et al., 2019). In fact, indigenous communities are largely responsible for discovering, utilizing, cultivating, and trading medicinal plants (Menendez-Baceta et al., 2015; Cámara-Leret et al., 2019). Accordingly, previous studies have identified positive correlations between cultural diversity and biological diversity (Gorenflo et al., 2012), and more specifically, between ethnicity and medicinal plant species richness (Caballero-Serrano et al., 2019). Consistent with these studies, we found that endemic medicinal plant species richness in China is positively correlated with both ethnic minority populations and with the ratio of ethnic minority population size to that of the total local population.

Larger altitudinal ranges usually contain higher environmental heterogeneity, which promotes higher biodiversity through the effects on ecological niches, climate refuges, diversifications (Stein et al., 2014). This environmental heterogeneity hypothesis is supported by previous studies that have shown that altitudinal range significantly affects the distribution of endemic plant species and endemic bird species in China (Feng et al., 2016; 2020). Our finding that there are significant and positive associations between altitudinal range and distributions of endemic medicinal plant species in China is also consistent with this hypothesis, and again emphasizes the crucial role of mountain regions in protecting China's high biodiversity.

4.5. Limitations of this study

There are several limitations of this study, which may be improved in the future studies. Firstly, a better indicator of cultural diversity is needed. Due to limitations of our data set, this study only used current population density of ethnic groups, which may not comprehensively reflect the effect of cultural diversity on distributions of endemic medicinal plant species. Secondly, a more precise resolution and detailed data set is needed. The current study is based on a data set at the prefecture city level, which is relatively coarse and limits the discussion of other important drivers at local scales. Thirdly, future studies should try to predict the effects of future global changes on the distribution of endemic medicinal plant species, which may inform conservation policies and practices.

5. Conclusions

In summary, this study found high species richness of endemic medicinal plants in southwestern China, which is a region rich in plant species, and has stable glacial-interglacial climate and high rainfall. In addition, the distribution of these endemic medicinal plants is affected by other factors, such as the cultures of ethnic minority groups in the region. These findings combined those of previous studies highlight the crucial role of southwestern China in the conservation of China's historically well-preserved biodiversity, especially in the context of unprecedented global climate change and anthropogenic activities.

Acknowledgements

LM was supported by National Natural Science Foundation of China (31870506) and Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDB31000000). GF was supported by the the National Key R & D Program of China (2019YFA0607103) and the National Natural Science Foundation of China (41861004).

Author contributions

G.F. and L.M. developed the idea; H.W. and L.M. collected and provided the data; G.F. and H.W. did the analyses; G.F., Y.X., H.W., Y.L., and L.M. wrote the paper.

Conflict of interest

These authors have no conflict in interest.