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Native useful vascular plants of China: A checklist and use patterns

Of all types of interactions between humans and plants, the utilization of plants by people is the most direct and influential. China has a long history of using native plants and a large body of recorded knowledge on uses. Here, we present an inventory of plant uses in China based on an extensive survey of the literature. Twelve categories of usage are recognized (medicinal, edible, etc.), these categories being chosen according to an integration of various current standards. A total of 50,521 use-citations were recorded, covering 10,808 species and infraspecies, representing 28% of the Chinese flora. Additional information is included in the dataset on taxonomy and endangerment status. Analysis of the data reveals that the eight plant families with the greatest numbers of species used in China, namely Asteraceae, Fabaceae, Rosaceae, Ranunculaceae, Poaceae, Lamiaceae, Orchidaceae, and Liliaceae, are also the top eight most species-rich Chinese plant families. However, there are some families that are over-represented or under-representation in certain use categories, compared with their relative abundance in the total flora. There are indications that rare and endangered species are being subject to some degree of over-exploitation. A disproportionately high number of used species are Chinese endemics (3552 species, representing over 33% of used species). A total of 20% of used species have been classified as threatened nationally or globally, according to at least one of the various threat assessments that have been made for the Chinese flora. This comprehensive inventory of the useful plants of China, with relevant ethnobotanical information included, provides a baseline for further studies of plant resources. It will be useful in follow-up research. The scientific dataset it contains will be useful for the protection and sustainable utilization of plant resources in China.


The importance of useful plants
Useful plants play a significant role in human living (Smekalova, 2012). Since antiquity, humans have used a great diversity of wild plants for food, medicines, fuel and many other purposes (Prance and Nesbitt, 2005;Tardio et al., 2006). Some plants discovered to be used in traditional medicine through ethnobotanical research have proved useful for the development of new drugs used for treating cancer, malaria, Alzheimer disease, HIV/AIDS and other diseases (Lentini, 2000;Butler, 2004;Newman et al., 2003).
Currently, more than 50% of all approved drugs contain natural products or their derivatives (Marrelli et al., 2015;Ovadje et al., 2015). There has been growing interest in finding the health functions from traditional medicines and wild fruits (Chen et al., 2006;Saleem et al., 2002;Leonti et al., 2006;Pieroni et al., 2002). Nowadays, the effective use of genetic resources of the planet is considered as a key factor in the pursuit of sustainable development around the world.

Close use relationship between humans and plants in China
China is among the world's richest countries in terms of plant biodiversity. One estimate is that there are some 33,000 vascular plant species (Jordi et al., 2006), but, according to our statistics, there are 39,174 species and infraspecies) recorded in all. There are 55 officially recognized ethnic minorities in China, more than 80% of them having their own traditional medicinal knowledge systems (Jia and Li, 2005). In addition to plants used in traditional medical systems in China, many ethnic minorities use a diversity of species in their folk medical traditions. Anthropological and ethnobotanical studies in China, initiated by Professor Pei Shengji in the 1980s (Zhang et al.,2018), have resulted in the compilation of much detailed information about the types and uses of native plants. There has been a concentration of such studies in those areas with the greatest indigenous and ethnic diversity, especially within Yunnan, Guizhou, Guangxi, Hainan, Inner Mongolia, Xinjiang, Tibet, Hunan and others areas (Table S3). There has also been much progress in follow-up scientific assessments and development of applications. Assessments through bioassays of the chemical molecules responsible for the traditional uses of plants have been undertaken from the 1950s (KIB, 2009) and, in consequence, a large number of compounds have been identified with potential for use in the pharmaceutical, cosmetic, food, agricultural and other industries. Many new drugs have been developed, such as artemisinin, total saponins of Panax notoginseng (Xueshuantong for injection), and so on have been successfully developed in China (Tu et al., 2015).
Of all types of interactions between human beings and plants, ethnobotanical studies of how plants are used has the most practical implications. Studies of useful plant can potentially progress through three research stages e field investigations and cataloguing, scientific assessment, and development of applications (Pei and Huai, 2007). The cataloguing of the field investigations is an important part of the first stage, which is also important for providing support for assessing and developing the management of plant resources.

Dispersed state of knowledge on plant uses and database construction
While information about the plant resources of China and their traditional and current uses has been documented for some areas, it is vastly dispersed and inadequately integrated. Due to the professional characteristics of scientific publications, most of the literature has only been published in small publication runs, many publications only being available to members of small research groups involved in diverse research fields such as botany, biology, chemistry, conservation biology and others (Javiera et al., 2019). Furthermore, some publications, such as unpublished theses and dissertations, are not widely accessible. Hence, the scattered nature of the data has prevented a full understanding of the current state of knowledge about the uses made plants in China. Previous analyses have been concerned with only subsets of the total potential dataset.
Since 2008, the Scientific Data Project of the Chinese Academy of Sciences has funded a program of digitization and database construction for the Chinese flora. This has included the cataloguing and integrating of information on uses. Although the online databases that have been compiled through this program have played an important role in the rapid spread of plant-related knowledge in China, further integration of useful plant information is needed.
While many publications about the Chinese flora have been produced over the years, the scientific names used for the same species can differ between them, as understandings of taxonomic relationships and the delimitations of species have changed. Many scientific names of plant species were revised during the preparation of the latest edition of Flora of China in English. The true identity of plants for which traditional uses have been recorded can become lost, leading to a loss of traditional knowledge in disguise (Ai, 2019;Qin and Tian, 2014). Therefore, research on the identity of useful plants is becoming a hot issue in China. We need a complete catalogue of useful plants matched to the latest taxonomic treatments and associated nomenclature. This will help promote a better understanding of value of biodiversity in China and enhance its usefulness for its protection and sustainable utilization.
Here, we present our results, providing: (1) a complete checklist of the useful plants of China, catalogued according to the nomenclature used in the latest edition of the Flora of China; (2) an analysis according to categories of usage, showing the general patterns of use of the Chinese flora; and (3) discussing the potential influence of plant use patterns on plant diversity in China.

Baseline checklists of Chinese plant diversity used in this study
The Chinese flora, according to Flora of China (2018), contains 39,174 vascular plant species and infraspecies belonging to 312 families. Generally, flora of China records the native plants in China. However, it also contains a small number of alien plant species closely related to human life, such as some crops. In this study, we take all the plants recorded in Flora of China as baseline of native Chinese plant diversity. These, listed with their synonyms, constituted the baseline checklist used in the present study.

Data sources, literature mining and databases construction
A useful plant in our study is defined as a plant used by people, following Hill (1937). We use the term "use-citation" for mention of a specific use of a particular plant species in a specific source (Javiera et al., 2019). Each use-citation includes a plant name, taxonomic information, usage and references. To begin our study, we consulted authoritative books about useful plants, such as the Pharmacopoeia of the People's Republic of China (CPC, 1953(CPC, -2015, Chinese Materia Medica (SATCM, 1999), Economic Flora of China (BLWP, 1961), etc. (Table S3), and digitalized the information into a structured data table. We followed up with literature searches of journal articles, reviews and theses on Chinese ethnobotany, as available in China. We used relevant keyword combinations, such as "ethnobotany", "Chinese traditional knowledge", "useful plant", "medicinal plant", "edible plant", etc., to retrieve information online from a total of 23 theses and 99 research articles (Table S3) to enter into our database. A taxon names indexing tool named Taxonfinder (http://taxonfinder.org) was used to detect scientific names in thousands of digital texts. Next plant usage terms, such as "medicine", "edible", etc., were used to interrogate the dataset on species used for different purposes.

Classification of uses and statistical analyses
Categories used for the recording of plant uses have changed with the progression of plant science. According to traditional economic values and uses, plants used as resources are divided into roughly 10e20 categories (BLWP, 1961;Zhu, 2004;Wang and Li, 2014;Chen et al., 2014). Wishing to refer to both these categories and the usage categories that are used in modern economic botanical and ethnobotanical studies, we decided to recognize 12 usage categories in total (Table 1.). Ours is a modified version of the classifications of use found in the Economic Flora of China (BLWP, 1961) and Plant Resources in China (Zhu, 2004). We entered the information on plant uses gathered from the literature into these 12 categories in our database. Statistical analyses were then carried out on the data in the database to determine the characteristics of the plants used, the frequencies of use of different species, the parts of the plants used, the numbers of use-citations per species and the frequencies of plant parts used. Linear regression was used to determine the relationship between the numbers of plant species used for any purpose and overall numbers of species per family and also, separately in the case of the use-categories of medicinal plants, edible plants and ornamental plants, to determine whether there were significant statistical differences in species used per family in these cases.

Results
A total of 50,521 plant use-citations was extracted from the literature on Chinese vascular plants. These were categorized into species, using nomenclature and current taxonomic understandings as in the Flora of China. Taking account of synonymies and misspellings, a total of 10,808 useful species was determined (28% of flora of China), belonging to 2276 genera and 284 families (Table S1). The number of useful species per use category was 9772 for medicinal uses, 2061 for edible uses, 1102 for ornamental or planting uses, 767 as industrial raw materials, 779 for timber, 692 for fiber, 547 with oilseeds, 752 for fodder, 183 for pesticides, 149 for religious or cultural uses, 129 for dyeing and 352 with other uses (classifiable into the foregoing categories (used as green manures, for handicrafts, toys, hobbies, tobacco, etc. (Table 1).
Of the useful plant species and infraspecies, 3552 (33%) are endemic to China, 1353 are included in at least one of the national threatened plant lists available for China and 1356 are included in at least one list of globally threatened species, such as those of IUCN and CITES. In all, 2106 of the species and infraspecies (20%) are included in at least one list of threatened plants, which is equivalent to a large proportion (30%) of the total number of Chinese threatened plant species. All use-categories contain rare and endangered species, the greatest number being for that of medicinal plants. A total of 3159 medicinal plant species are endemic, 418 are recorded in the Chinese Plant Red Data list (accounting for 19% of the total Red Data list), 315 on CITES and 1154 have been Red-Listed by IUCN (Table 2). Table 1 Use-categories used for categorizing uses of the Chinese useful flora, with definitions of each category, numbers of species and use-citations per species and the percentages of the total Chinese used flora belonging to each category.

Usage
Abbr. The number of useful species in a plant family and the total number of species in that family are significantly related in China (Fig. 1). Those families with higher species richness are likely to have higher numbers of useful plants. Tests on the relationships between the number of species per family and the use-categories of 'medicine', 'edible' and 'ornamental or planting' as the dependent variable revealed all to be significantly related (Adjusted R Square > 0.5, P < 0.05). Table S2 shows the numbers of species in each use category for each family. Table 3 shows the data for the top five most speciesrich families in each use category. Table 4 summarizes the results of regression analyses for 'all uses', 'medicine', 'edible' and 'ornamental or planting'. The families included are those that contain much higher or lower numbers of useful species (over 3.00 or under À3.00; P < 0.01) than predicted by chance.
Of the total of 39,174 plant species and infraspecies in the Flora of China, 28,366 (72%) have no recorded uses, 7494 (19%) have one recorded type of use, 1692 (4.3%) have two, 821 (2%) have three and the remaining 801 (2%) have more than three recorded types of use. There is an approximately negative exponential function model between the numbers of used species to use categories (Fig. 2).
There are significantly more use-citations for species in the 'medicinal' and 'edible' categories than for species in the other categories of use (Fig. 3).
Of the total of 50,521 use-citation records assembled, the most commonly used parts of plants are root, stem, whole plant and leaf, all with more than 11,000 records of use (Fig. 4). Fruits, flowers, seeds and above-ground parts are used to lesser extents.

High number of plant species used in China
The total number of Chinese species and infraspecies of vascular plants used is 10,808, the corresponding percentage of the total flora (28%) being similar to that recorded for countries such as Chile (23%), Mexico (23%) and Ecuador (30%) (Javiera et al., 2019). Of the total for all uses, 9772 species and infraspecies have been recorded as medicinal. After adjusting for taxonomic revisions, this figure is not dissimilar to the early estimates of nearly 11,000 species reported to have been used since the Paleolithic period (Hamilton, 2004), the estimated 12,000 species estimated to have been used by Academician Xiao Pigen (Li, 2008) and the about 8000 species recorded as medicinal in the ten volumes of Chinese Materia Medica (1999). For edible plant resources, Ministry of Agriculture (1995) reported that China had at least 400e500 wild species of vegetables and more than 200 wild species of starch or sugar plants. Our summary found that totally 2061 plants were recorded with edible usages (Table 1) (Table 1). Our own inventory of useful plants has the advantage, compared with previous inventories, of including all published information available in China on uses of plants in China, which should be useful for those making efforts to achieve sustainable utilization of the plants.

The endemic and threatened status of plant species used in China
Overexploitation is a major threat to plant diversity (Corlett, 2016) and thus a special conservation concern with respect to  used species and especially for species that are national endemics.
Our figure for the total number of endemic species used medicinally (3159) ( Table 2) is roughly similar to that of 3510 reported earlier by Li et al. (2017). However, the result from our own inventory that about 19% of species included on the Chinese National Red Data List are medicinal is greatly different from the estimate of Huang et al. (2011) that 60e70% of Chinese endangered species are of medicinal value. The explanation may be that the lists of endangered plants given in different sources are not the same and that there are differences of opinion about which plants are medicinal. In general, a notable proportion (25% of endemic plant, and 18%e22% of each endangered category) of the rare and endangered plants species have been used in China, that indicate that rare and endangered species are being subject to some degree of overexploitation. We suggest that before endangered species are utilized, especially before commercial operations, more research on domestication and cultivation should be carried out. Sustainable utilization of plant resources requires coordination of protection and development.

Overall use patterns of plants in China
Globally, families of plants with greater species richness are more likely to have more useful plants (Javiera et al., 2019). Linear regression confirms this is the case for China (Fig. 1). The dominant families of Chinese flora, such as Poaceae, Asteraceae, Fabaceae, Liliaceae, Ranunculaceae and Chenopodiaceae contain a greater number of used plants. Our statistics show that most plant species used in China are used for only one or two categories of use (Fig. 2), whereas a few plants species have multiple usages, such as for medicine, food, ornamental, construction material, etc. The latter, which include Betula platyphylla, Ulmus macrocarpa, Ficus microcarpa, Vitex negundo, Cinnamomum camphora, Broussonetia papyrifera, Sophora japonica and Bischofia javanica, have greater overall potential for utilization and development and should be given more attention in follow-up studies. The fact that the number of used species per use-category confirms approximately to a negative exponential function indicates that most of published floras for China (which are often for only limited area) are deficient in how many species are actually used. We are still at a relatively initial stage in compiling a full list of used plants at the national scale.
We recorded a total of 50,521 use-citations. The most used parts of plants (each with over 11,000 citations) are roots, stems, whole plants and leaves. The first three of these collection modes will cause considerable damage to the plants, which has a certain pressure on the sustainable utilization of wild plant resources (Zhuang and Wang, 2009).
Wild medicinal and edible plant resources are widely used in China, especially in ethnic areas. In our inventory, medicinal and edible plants were the two main use categories, using respectively, 90% and 19% of all species in the Chinese used flora (Table 1).

Rich diversity of medicinal and edible plant species in China
Benefiting from the inheritance of traditional Chinese medicine (TCM), China uses more plant species as medicines (9772) than any other country. The proportion of the national flora used medicinally (25%) is greater than has been recorded for other countries, such as Chile (12%; Javiera et al., 2019), Argentina (14%; Barboza, 2009), Mexico (7%; Javiera et al., 2019) and the USA (13%; Moerman, 1991).
Medicinal and edible plants have significantly more numbers of use-citations (3.62 and 2.21) than other categories of plant use (Fig. 3). The richness of traditional knowledge about medicinal plants and edible plants in China has been quantitatively confirmed in this study. Of the total of 50,521 use-citations of all uses, 37,523 (74%) are for medicinal use and 5163 (10%) for edible. It also suggests that researchers mainly focus on these two categories of resource plants, and we should pay more attention to other types of plant resources in the future.

Over-representation of some taxa in certain use-categories
Many studies have found that useful plants are not randomly distributed across floras. (Forest et al., 2007;Lulekal et al. 2011;Weckerle et al., 2011Weckerle et al., , 2012. Our study reveals that the same is true of China (Table 4).
Of the about 312 plant families present in the flora of China, the most over-represented in terms of useful species are Rosaceae, Ranunculaceae, Lamiaceae, Liliaceae and Fabaceae. They have the highest residual values in regression analyses (Table 4). Conversely, Poaceae, Cyperaceae, Athyriaceae, Dryopteridaceae, Orchidaceae and Ericaceae have lowest residual values such analyses, indicating that they have the lowest proportions of used plants.
In addition to regression analyses of family representation regarding all uses, separate regression analyses undertaken for particular uses reveal that Ranunculaceae, Lamiaceae, Rosaceae, Asteraceae, Fabaceae and Liliaceae are over-represented for use as medicines, Rosaceae, Liliaceae, Moraceae, Fagaceae and Poaceae for use as foods and Poaceae, Fabaceae, Clusiaceae, Rosaceae, Arecaceae and Cupressaceae as ornamentals.

Conclusions
Our main finding is that China has a large number of useful vascular plants. Our research into the literature has revealed that a total of 10,818 species and infraspecies have been used, with quantitative information now available on details about patterns of use. The close utilization relationship between the Chinese people and the Chinese flora is confirmed. More species have been used medicinally than in any other country. Those plant families that are richer in species in China contain a higher number of used plants, but there is over-or under-representation for certain usecategories, which suggests that, in these cases, the selection of species for use is non-random. Data are provided on the proportions of rare and endangered plants used. We have presented the first comprehensive ethnobotanical for Chinese plants. This will provide a baseline for further studies and provide insights into the selection of plant species for research, including to support scientific efforts made to protect and sustainably use the plants of China.

Author contributions
YHW contributed to the conception of the study. HFZ performed the data analyses and wrote the manuscript. YNW contributed to the dataset integration and database construction. CW, RH, JT and ZHL contributed to the ethnobotanical data collection.

Declaration of competing interest
We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.