Ex situ Flora of China
Hongwen Huang, Jingping Liao, Zheng Zhang, Qingqing Zhan     
South China Botanical Garden, Chinese Academy of Sciences, International Association of Botanic Gardens, China
Abstract: The role of living collections-based research and discovery has been a prominent feature throughout the history of evolution and advance of botanical science:such research is the core and soul of the botanical gardens. Currently, there are c. 162 Chinese botanical gardens, harboring c. 20, 000 species in China. As an example of initiatives to utilize the garden cultivated flora to address plant diversity conservation and germplasm discovery for sustainable agriculture and the bio-industries, the Ex situ Flora of China project aims to catalog and document this mega-diversity of plants that are cultivated in the Chinese botanical gardens. The concept of Ex situ Flora of China is a complete new formulation of species, based on garden cultivated individuals and populations, to obtain better morphological descriptions, provide multipurpose applicability and a fundamental data service that will support national bio-strategies and bioindustries. It emphasises integrative information, accurately collected from living collections across different Chinese botanical gardens, on biology, phenology, cultivation requirements and uses of plant resources, which are normally not available from traditional Floras based on herbarium specimens. The ex situ flora should provide better information coverage for taxonomy, biological and introduction and collection data and color photos of stems, leaves, flowers, fruits and seed, as well as useful information of cultivation key points and main use of each plant. In general, the Ex situ Flora of China provides more useful information than the traditional Flora Reipublicae Popularis Sinicae. The project of Ex situ Flora of China is planned to be one of the most important initiatives of the plant diversity research platform for sustainable economic and social development in China.
Keywords: Botanical garden    Living collections    Ex situ conservation    Botanical sciences    Cultivated flora    
1. Introduction

In the history of botany during the past 500 years, the botanical garden, as a specialized research institution of botany, has always been in the mainstream of botanical research, conservation and discovery of uses of plant resources. The botanical garden has a profound scientific connotation, with a comprehensive engagement in the basic biological research on plant, collections and the evaluation, exploration and sustainable utilization of plant resources. In particular, the role of living collections-based research and discovery has been a prominent feature throughout the history of evolution and advance of botanical sciences. Botanical research is the core and soul of the botanical gardens. Much of the historical literature has recorded that botanical gardens and living collections were inspiring places and research resources which had inspired many great scientists, such as, Carl Linnaeus (1707–1778), Charles Darwin (1809–1882), Gregor Mendel (1822–1884), Liberty Hyde Bailey (1858–1954), and Barbara McClintock (1902–1992), etc.

There are about 3000 botanical gardens in the world, widely across different climatic zones and floristic regions. Most importantly they provide habitats for > 120, 000 vascular plants in ex situ cultivation, accounting for about a third of known world plant species, including many economically important taxa or groups, such Aceraceae, Ericaceae, Fagaceae, Leguminosae, Magnoliaceae, as well as a large number of crop wild relatives, medicinal and aromatic, and ornamental plants. This ex situ cultivated flora contains an enormous amount of plant diversity in many well documented living collections in different botanical gardens and plays a critical role in maintaining the security of plant diversity, and in conservation, sustainable agriculture and other related bio-industries.

Currently, there are c. 162 botanical gardens in China (Fig. 1), harboring c. 20, 000 species in China (Huang and Zhang, 2012). As an example of initiatives to utilize the garden cultivated flora to address plant diversity conservation and germplasm discovery for sustainable agriculture and the bio-industries, the Ex situ Flora of China project aims to catalog and document this mega-diversity of plants that are cultivated in the Chinese botanical gardens. The project of Ex situ Flora of China is planned to be one of the most important initiatives of the plant diversity research platform for sustainable economic and social development in China (Huang, 2011).

Fig. 1 Map of distribution of Chinese botanical gardens.

China probably has one of the largest garden cultivated floras in the world. Even dated back to centuries ago when many western plant hunters (such as Pehr Osbeck during 1750–1752; Robert Fortune 1842–1861; Augustine Henry 1882–1890; Ernest Henry Wilson 1876–1930; George Forrest 1904–1932; Joseph F. Rock 1922–1949, etc.) were exploring in China, their first impressions was the huge garden cultivated flora, which was mostly grown in numerous private Chinese traditional gardens a century ago. Nowadays, botanical gardens in China have played key role for plant conservation, and a huge garden cultivated flora has been assembled in the past century (Huang and Zhang, 2012). However, unfortunately no national list or inventory of garden cultivated plants exist in Chinese history, even if many kinds of native Chinese plants that provide food, utility, and pleasure have been widely recognized worldwide. Ernest H. Wilson dubbed China the 'Mother of Gardens' because 'anywhere in the temperate zone of the northern hemisphere, no garden does not cultivate several species derived from Chinese plants' (Wilson, 1929). Today gardens and parks throughout the world showcase flowering plants like rhododendrons, camellias, magnolias, peonies, primroses, viburnums, and many others that originated in China.

Obviously, we need accurate information pertaining to plants found growing in China, both native and introduced. A complete inventory of garden cultivated plants and project of Ex Situ Flora of China should provide needed supports to future of these scientific and concomitant databasing efforts, along with other national mega-databases and contribute to China's national strategies of sciences and technologies in 21st century, as well as in accordance with China's government commitments to the Convention on Biological Diversity.

2. Concept and vision of Ex situ Flora of China

When we began formulating a strategy and project planning, the project concept differed from other known projects including the six-volume European Garden Flora, a project whose six volumes were published 1998–2000 and second edition released in 2011 (Cullen et al., 2011). The project of Ex situ Flora of China is different from the European Garden Flora, in at least these five aspects: 1) The initiation of Ex situ Flora of China is a state funded project aiming to a complete inventory of garden cultivated plants of Chinese botanical gardens but the renewed project continued into the Ex situ Flora of China while European Garden Flora started as a group of botanists on a voluntary basis for accurate identification of cultivated ornamental plants found growing in Europe; 2) starting point of raw materials, database and information are significantly difference. Ex situ Flora of China started with documented databases from the national inventory of garden cultivated plants in China while European Garden Flora initiated with catalogs or other similar materials and data from many European nurseries; 3) the priority Ex situ Flora of China is mostly on plants native to China where majority of plants found growing in the country is native while majority of plants found growing in Europe is exotics or introduced from other parts of the world; 4) The project of Ex situ Flora of China has an obvious advantage of availability of Flora Reipublicae Popularis Sinicae (FRPS, Chinese version flora of China) and Flora of China (an updated English version of FRPS) as benchmark while European flora is not such complete during compilation of European Garden Flora; 5) Ex situ Flora of China has formulated an integrative editorial strategy for inclusion of taxonomic information, natural distribution, morphological descriptions from living collections, passport information, and phenological and biological information and cultivation information while European Garden Flora is mostly a checklist of plant names and concise descriptions.

Our core concept of Ex situ Flora of China is a complete new formulation of species found in living collections, based botanical garden cultivated individuals and populations to obtain better morphological descriptions, and provide multi-purpose applicability and a fundamental data service that will support national bio-strategies and bio-industries. It emphasises integrative information, accurately collected from living collection across different botanical gardens in China, on biology, phenology, cultivation requirements and uses of plant resource, that are normally not available from traditional Floras based on herbarium specimens. The ex situ Flora should provide better information coverage for taxonomy, biological and introduction and collection data and color photos of stems, leaves, flowers, fruits and seed, as well as useful information of cultivation key points and main use of each plant (Fig. 2). In general, the Ex situ Flora of China provides more useful information compared with the traditional Flora Reipublicae Popularis Sinicae.

Fig. 2 Example of information included for each species and format in Ex situ Flora of China.

The formulation of the Ex situ Flora of China has obvious advantages and unique features that differ from other garden Floras or cultivated Floras, for example, the delimitation of species boundaries is also flexible, allowing for the possible inclusion of a list of cultivars for some species of special horticultural or ornamental interest, such as lotus, chrysanthemum, Rhododendron, etc. of which many cultivars have been developed from single species. The project also conforms to the trends of national and international ex situ conservation, public awareness and education and is consistent with the principle of long-term accumulation of biological data as well as in line with the country's strategic planning needs for baseline data converge.

In practice, the Ex situ Flora of China should provide significant support to botanical research and plant germplasm discovery and sustainable use: 1) Enhancement of taxonomic research with common-garden-based living specimens. The morphological and biological data collecting from living collections of different botanical gardens should provide both adequate and accurate descriptions and the delimitation of difficult taxa where traditional taxonomic revisions were based on herbarium specimens; 2) Support of comparative biology and frontline plant science research: for example, with increasing awareness of environmental and habitat changes in the overall context of climate change on plant distributions in situ, the Ex situ Flora project should provide intensive plant biological information from different botanical gardens across a wide spectrum of different latitudes, regional climates and habitats in relation to research on species' adaptive evolution, plant migration and distribution shifts and physiological or/and biochemical changes, etc.; 3) Strengthening germplasm discovery and sustainability of plant resource, which should enhance our current ongoing efforts in the case of medicinal plants, industrial bio-energy plants, landscaping and ornamental plants, new functional fruits and vegetables, environmental meliorating plants, etc.

The Ex situ Flora of China Project will include c. 300 families, > 3000 genera and approximately 16, 000–20, 000 species from ex situ living collections across 30–60 botanical gardens in China (Huang, 2014, 2015–2017). Both electronic and hard copy versions are simultaneously available, with the e-version periodically updated. Hard copy publication has been arranged by large families or genera and combined small families. A total of approximate 80 volumes are expected within time frame about 15–20 years.

Our vision for the ex situ Flora is that although initiated as a national project for China, it might eventually become an ex situ Flora of the world after the successful completion of the Chinese ex situ Flora and regional ex situ Floras such as an Asian ex situ Flora because the concept of the Ex situ Flora of China is versatile and adaptable to any scale.

3. Comparisons between Ex situ Flora of China and Flora Reipublicae Popularis Sinicae

The project of Ex situ Flora of China should have benefits for both scientific research and applications of using plant resources. Documenting the data well collected from sites of ex situ living collections across different botanical gardens would enhance both traditional botanical research and frontline research which largely depend on sufficient and accurate data of plant growth and development, such plant taxonomy and climate change biology. In particular, phenological data of many plants collected from different botanical gardens in different latitudes and longitudes would provide solid evidence of climate changes over decades and centuries. Meanwhile, the formulation of Ex situ Flora of China is largely designed for supporting plant resource exploration and utilization and for services provided by importance of plant resources for human survival and sustainability, such as wild relatives for crop breeding and genetic improvement, resources for new specialist crops, local indigenous plants for reforestation and wetland restoration, biodiesel plants and medicinal resources, etc. which are highly valued in China.

Nevertheless, Ex situ Flora of China is different from traditional Flora Reipublicae Popularis Sinicae in many aspects:

3.1. Exotic plants

The 10 largest families in ex situ cultivation are these commonly seen families in China, i.e. Orchidaceae, Poaceae, Rosaceae, Fabaceae, Asteraceae, Liliaceae, Arecaceae, Euphorbiaceae, Cactaceae and Asclepiadaceae. However, two families, Cactaceae and Arecaceae, are non-native. Obviously, all species of Cactaceae were introduced from desert areas of other parts of the world, whereas more than 90% species in Arecaceae came from South America. In comparison, the 10 largest families in Flora of China (FOC) are Asteraceae, Poaceae, Fabaceae, Orchidaceae, Rosaceae, Ranunculaceae, Lamiaceae, Ericaceae, Cyperaceae and Liliaceae, six of them are the same top ten in ex situ conservation. The Flora of China has some unique features, such as the 10 largest families of FOC accounting for > 1/3 of the total number of Chinese native plant, that is c. 12, 404 out of 31, 365. About two thirds of the 312 families contain 50 or fewer species, i.e. 212 families in China contains only c. 900 out of 31, 365 (2.9%), average c. 23 species/family. Many other families also contain alien plants introduced form other countries.

Nonetheless, an inventory of garden flora of China showed a relative low percentage of exotic species in China (Huang and Zhang, 2012), i.e. about 10% of total number garden cultivated species, which is quite different from the situation in US and Europe. The possible explanation is that China is rich in plant diversity and has approximately one and a half and twice as many vascular plants than US and Europe, respectively. North America and Europe have been active in plant hunting and introduction of plants from over the world in past 400–500 years. In fact, there are 3–4 times more introduced plants than native plants in the US (Elias, personal communication) and same probably is true in Europe (Table 1).

Table 1 Comparison of 15 largest families between in Ex situ Flora of China and in Flora Of China.
Ex situ Flora of China Flora of China
Family name Number of species Family name Number of species
1 Orchidaceae 702 1 Asteraceae 2165
2 Poaceae 639 2 Poaceae 1906
3 Rosaceae 629 3 Fabaceae 1710
4 Fabaceae 574 4 Orchidaceae 1378
5 Asteraceae 495 5 Rosaceae 954
6 Liliaceae 477 6 Ranunculaceae 941
7 Arecaceae 405 7 Lamiaceae 900
8 Euphorbiaceae 356 8 Ericaceae 861
9 Cactaceae 352 9 Cyperaceae 825
10 Asclepiadaceae 326 10 Liliaceae 764
11 Zingiberaceae 303 11 Scrophulariaceae 704
12 Rubiaceae 301 12 Apiaceae 636
13 Lamiaceae 274 13 Dryopteridaceae 589
14 Lauraceae 265 14 Saxifragaceae 572
15 Gesneriaceae 264 15 Lauraceae 543
3.2. Importance of economic and useful plant species

The 15 largest genera in ex situ cultivation are mostly economic and useful plant species, including those of horticultural, medicinal, industrial raw materials and other economic value, such as Hoya, Begonia, Rhododendron, Ficus, Rubus, Camellia Euphorbia, Aloe, Acer, Dendrobium, Ilex, Rosa, Berberis, Bulbophyllum, and primulina (Table 2). In contrast, four largest genera from the 15 largest genera in Flora of China are the same of those in ex situ. The 15 largest genera of wild species in nature include 4642 species, accounting for c. 15% of the species in the Flora of China. In fact, the 45 largest genera with over 100 species include more than a quarter of the total species of the native flora. In addition, c. 1283 out of a total 3329 genera consist of only a single species. Evidently, the Ex situ Flora of China highlights much more economic and valuable species.

Table 2 Comparison of 20 largest genera in the Ex situ Flora of China and the Flora of China.
Ex situ Flora of China Flora of China
Genus name Number of species Genus name Number of species
1 Hoya 202 1 Rhododendron 570
2 Begonia 201 2 Carex 505
3 Rhododendron 155 3 Corydalis 364
4 Ficus 122 4 Pedicularis 363
5 Rubus 114 5 Astragalus 355
6 Camellia 104 6 Primula 304
7 Euphorbia 102 7 Salix 282
8 Aloe 98 8 Saussurea 274
9 Acer 98 9 Gentiana 254
10 Dendrobium 92 10 Impatiens 254
11 Ilex 91 11 Saxifraga 239
12 Rosa 91 12 Berberis 216
13 Berberis 86 13 Aconitum 211
14 Bulbophyllum 81 14 Rubus 209
15 Primulina 76 15 Ilex 208
16 Carex 70 16 Dryopteris 199
17 Aechmea 63 17 Artemisia 189
18 Viburnum 63 18 Begonia 188
19 Dryopteris 62 19 Athyrium 180
20 Polystichum 62 20 Oxytropis 177
3.3. Taxa entry and boundary

The principles for inclusion and circumscription of taxa have been well formulated and standardized. The Ex situ Flora of China is species based inventory and documents living collections in botanical gardens. Unlike other cultivated floras, a large percentage of cultivars have to be included. A typical example is the Cultivated Flora of North America, a project initiated 2001 but terminated in 2006. Difficulties and impediments experienced by the project are obvious, including the fact that more introduced than native species exist in North America, and that there is a large percentage of cultivars and disagreement between taxonomists or botanists and horticulturists or agriculturists on which taxa to include and how they should be delimited, as well as insufficient financial support, etc. (Elias and Raven, personal communication). In the initial guidance of the Ex situ Flora of China during early stage of project planning, species level entry has been officially determined so as to exclude cultivars under any terms, although a list of cultivars might be allowed as an appendix in some special horticultural species.

However, in view of the unique situation of ex situ living collections, below species level, subspecies and varieties or forms are accepted with strict definitions and terminology, which are more appropriate for some families and genera in ex situ cultivation because the Ex situ Flora of China is partially driven by applications of plant germplasm evaluation and discovery. In any cases, voucher specimens are required and collecting and depositing voucher specimens of each taxon entry have well formulated and guided.

All species entries are referenced from Flora Reipublicae Popularis Sinicae and Flora of China for verification of taxonomic names. However, taxonomic treatments in some families and genera are different between the earlier Chinese version of Flora Reipublicae Popularis Sinicae and the updated English version of Flora of China, and also controversies exist regarding species names found between plants in Floras and living collections due to many taxonomic revision made after plants were brought into ex situ cultivation. In such cases, prioritized references are recommended, with the Flora Reipublicae Popularis Sinicae having highest authority for species name verification because it is more accepted by Chinese botanist and gardeners. In documenting and data collecting process for any families and genera of the Ex situ Flora of China, publishing new taxa, new combinations and new names are discouraged unless there are substantial studies conducted in natural populations in the wild and sufficient evidence is obtained.

3.4. Passport data

Passport data have been considered as critical information for an ex situ Flora because this information provides important indications of origin, time, locality, geographical data and some habitat information, as well as important historical information on vegetation and environment. The design and inclusion of this data differentiates other checklists like garden Flora or cultivated Flora for better information for various users in the botanical, forest, agricultural, horticultural, industrial, private sectors, etc. in line with our concept or principle of multi-purpose services as an end product. In principle, the passport data is a mandatory requirement in the Ex situ Flora of China, and in turn enforces participating botanical gardens to enhance their data management ability and capacity building and higher standard botanical garden management, although difficult exist for many historical introductions and those plants introduced in past decades.

Although botanical gardens in China began to pay attention to records and data management of living collections from the 1960s (Yu et al., 1965), it has never reached a proper level in a standardized, uniform and persistent maintenance. For example, a recent survey shows that only 48% of Chinese botanical gardens (78 of the total 162 gardens) have maintained collecting records (Huang, 2017). The Ex Situ Flora of China is designed to rescue historical data, both of living plant accessions and ex situ cultivation to promote a collection strategy and standardize ex situ management of living conservations, in particularly with emphasis on documenting of material types collected, provenances, sampling methods and health status of living plants, and garden conservation policies. One of the primary functions of the living collections is to provide a reference source of correctly named plants for taxonomy, horticulture and many other purposes and the Ex Situ Flora of China will also have a further focus on morphology and taxonomic verification, cultivation techniques, and sustainable utilization of plant resources based on 'common garden' conditions, which will eventually improve the management and quality of living collections and enhance scientific and research values and the efficiency of ex situ conservation.

3.5. Phenological data

Inclusion of phenological data for each entry is probably an idealistic goal but requires that the role of botanical gardens in accumulating data for research into climate change biology is a key goal for long term planning. The basic idea is that a number of botanical gardens should engage in studying and monitoring the phenology and adaptive changes of certain keystone species in ex situ living collections. The data collected across different botanical gardens in different latitudes, longitudes and elevations would provide solid biological evidence of climate changes and plant adaptive response and important real data from living collections supports long term monitoring climate change biology.

For example, Magnolia cylindrica E. H. Wilson originally occurred in Anhui, Zhejiang, Jiangxi and Fujian provinces, and was cultivated in at least seven botanical gardens since 1980s. Its passport data and phenological data were documented from the seven botanical gardens. The phenological data showed that spring phenophases (budburst and leafing) were mostly consistent with changes of latitudes, c. 7 ± 3 days in every latitude (Yang et al., 2015). However, some species have multiple individuals in ex situ cultivation and showed large variation of phenophases, e.g. more than 20 days difference even in the same habitat. For example, Rhododendron fortunei in Lushan Botanical Garden exhibited variation of flowering time ranging from end of April to mid of May. Thus, calibration of individuals for monitoring and collecting phenological data would be important measure to be taken such as labeling individuals for phenological data collection or even cloned genotypes in different gardens for quantity control of rigid phenological data for Ex situ Flora across botanical gardens. BBCH codes (Germany; Meier, 2001) may be adopted as standards and guidelines for phenological observation.

3.6. Taxonomic system

The Flora Reipublicae Popularis Sinicae (FRPS) and updated English revision Flora of China (FOC) are important references for the Ex situ Flora of China and provide basic information benchmark for taxonomic system and systematic arrangement of Chinese plant families. Therefore, the Ex Situ Flora of China inherits the systematic arrangement of angiosperm families of the FRPS and FOC as benchmark reference and also adopted Engler's system for angiosperms (1964), Ching's system for pteridophytes (1978) and Cheng's system for gymnosperms (1978) in consistency with FRPS and FOC. However, reasonable adjustments in individual genera or species treatment are encouraged based on the latest rational revision of some families with advanced botanical research. While systematic arrangements of genera within a family or species within a genus are also in principle consistent with those in FRPS and FOC, phylogenetically primitive groups should be placed before the advanced groups, closely related groups in evolution should be arranged together, or follow the latest monographic systematic research. In the compilation of each volume of the Ex situ Flora of China taxonomic revisions have been encouraged to reflect advances of new information from the Ex situ flora. To verify each accepted name and taxonomic status of living collections, besides database FRPS and FOC, additional references are also available from the Chinese Field Herbarium (http://www.cfh.ac.cn/default.html), Tropicos (http://www.tropicos.org/) and The Plant List (http://www.theplantlist.org/). Although the Angiosperm Phylogeny Group System (APG) has advanced and made many changes to the circumscription and placing of several families and consequently of many genera, the Ex situ Flora of China might not necessarily compromise the concept and principles in this early stage. APG Ⅲ or higher version might need to be adopted in certain circumstances in later stage.

4. A three-phase planning strategy 4.1. Checklist of ex situ cultivated plants in China

Since the Ex situ Flora of China is a long term project, a three-phase outputs of project have been formulated and implemented. The checklist of ex situ cultivated plants in China was the first phase output of the Ex situ Flora of China and published in 2014 as a benchmark of the project.

The checklist mostly reflected results of the inventory of garden cultivated species of living collections across Chinese botanical gardens. It lists 15, 844 species (including 179 subspecies, 940 varieties, 74 forms) belonging to 314 families and 3182 genera. Pteridophyte plants based on Qin's system (Ching, 1978) are consist of 59 families, 167 genera, 835 species (including 26 subspecies, 1 varieties and 5 forms), gymnosperms based on Cheng's system (Cheng et al., 1975) comprise a total of 12 families, 54 genera and 299 species (including 29 and 1 form) whereas angiosperm plants according to Engler system (Diels, 1936) account a total of 243 families, 2972 genera and 14, 710 species (including 180 subspecies, 877 varieties and 67 forms).

Although tremendous efforts have invested in the checklist for taxonomic accuracy of each entry with both software screening and experts manual checking, some inaccuracy and mistakes are still be unavoidable due to the complications of using historic handwritten records of ex situ data and management of different gardens, and conflicts between ex situ records and changes from recent revision and treatments of many taxa. Thus, there are remaining 2000–3000 species not included in the checklist because of controversy of taxonomic treatments, or not yet explicitly described but tentatively designated as questionable species, etc. With the Ex situ Flora of China each family or genera volumes in progress, those uncertain species will be resolved in future. 'Completion of the checklist of ex situ cultivated plants of China is the beginning of the Ex Situ Flora of China and the checklist is the key to opening the floral world of the country' (Zhang, 2015).

4.2. Encyclopedia of Chinese garden flora

The second phase of the three planned outputs the Ex situ Flora of China was implementing and completion of 13-volume Encyclopedia Chinese garden flora by 2017 (Table 3). As a curtain-raiser for the Ex situ Flora of China, the encyclopedia aimed concise formatting each species consisting of brief text description with color photographs from living collections for brief and clear illustration of main features of each species. The contents mainly include the Chinese name, Latin name, brief text of identification feature and an on-site photograph of living plant. These 13 volumes Encyclopedia Chinese garden flora are equivalently comparable to European garden flora in terms of contents, but with addition of more living collection based feature descriptions and color photographs for each entry.

Table 3 Volumes of encyclopedia Chinese garden Flora.
Volume Families range Amount Year
Family Genus Species
1 Acanthaceae – Aquifolianceae 15 228 1008 2015
2 Araceae – Basellaceae 8 238 1177 2017
3 Begoniaceae – Cactaceae 16 183 1187 2016
4 Callitrichaceae – Convolvulaceae 23 306 1125 2017
5 Coriariaceae – Eucommiaceae 30 166 1103 2017
6 Euphorbiaceae – Gramineae 9 327 1546 2015
7 Guttiferae – Leguminosae 21 338 1458 2017
8 Lemnaceae – Myoporaceae 22 230 1293 2017
9 Myricaceae – Phytolaccaceae 26 249 1232 2017
10 Piperaceae – Rosaceae 22 163 1346 2017
11 Rubiaceae – Symplocaceae 26 314 1180 2015
12 Taccaceae – Zygophyllaceae 22 197 1280 2017
13 Pteridophytes and Gymnosperms 71 229 1291 2016
Total 311 3168 16, 226

However, in view of long history and original records of ex situ living collections, some entries are not synchronized with updated taxonomic revisions so that the editorial strategy of encyclopedia has been insisting on the principle of 'respect historical facts and move with the times', and some taxa have reasonably been adjusted and combined according to updated revisions of systematics.

The encyclopedia Chinese garden flora comprises one volume for ferns and gymnosperms (Volume 13), 12 volumes for angiosperms (volumes 1–12), all arranged in alphabetical order by the Latin name of families. In each volume, each family is also arranged alphabetically by the Latin names of genera and species. For convenient access, all books are indexed by Chinese plant names and Latin names. A total of 16, 226 species belonging to 311 families and 3168 genera are included in the encyclopedia (Table 3).

4.3. First two volumes of Ex situ Flora of China

The third phase of the three planned outputs of Ex situ Flora of China is the core component of the project. So far two family volumes have been published, Magnoliacease with 11 genera and 147 species (including 1 subspecies, 7 varieties and 3 hybrids); Myrsinaceae with 6 genera and 90 species (including 1 variety). These two out of approximate 80 volumes in next 15–20 years or even longer time frame have been considered a pioneer volumes and trials of compilation formats.

In the documentation and editorial process of the first trial volume of Magnoliaceae, particularly, many lessons have been learned that will lead to better understandings of status and facing problems of ex situ flora and garden living collections so that implementations of other volumes of the Ex situ Flora of China can be better organized in more focused efforts in future. Many difficulties and data bottlenecks need to be overcome such as:

1) Incomplete or missing introduction records and passport data

2) Undocumented or imprecise geographical provenances

3) Data management not standardized

4) Inadequate taxonomic information and species identification

5) Lack of continuity of phenology observation and incomplete phenology data

6) Lack details of description of plant growth and development data

To address these problems, measures have been taken to improve the situation so that details of compilation and editorial guidance are formulated at the beginning stage of each family volume when the editorial committee and compilation research group are organized because each family volume will take about 3–5 years or even longer. Currently 30–40 family volumes are organized and compilation research groups established.

5. Challenges and prospects

Ex situ Flora of China is multi-decade project. Although project initiation and progress in early phase are very promising and have attracted much interest from both the botanical field and botanical gardens communities as well as the public. However, the project is still facing many challenges.

First, standardization of format and data collection across different taxa ranging from ferns to timber trees and across different gardens localities ranging from tropics to frigid is quite challenging although much detailed guidance has been given and many discussion meetings organized. Further gap analyses and more precise formatting are needed so that editing guidelines are more specifically established and all terminology, both scientific and botanical garden technical should be precisely defined. For example, many medicinal plants have special features linked with functional medicinal parts, in turn collecting morphological data need be modified to benefit to end users. Another example is the need to describe both male and female flower morphologically in dioecious species.

Second, the collection of phenological data aims to contribute to climate change research and monitoring climate changes over decades or centuries within botanical gardens settings. However, standardized protocols for a wide range of different latitudes, longitude and elevations of data collection are crucial for efficiency of monitoring and data quality. Besides many criteria of data standardization can be adopted from International Phenology Gardens (IPG) project, there are still many challenges on data collection from botanical gardens located in different latitudes in China. For example, flowering difference of different provenance of same species can be various as long as 10 days. Some different genotypes of same species can even have different flowering periods of up to two weeks, Apparently, standardized genotype or provenance with correction of statistic standard error are important criteria and practice for phenology data.

Third, coordination between botanical gardens is a top organizational bottleneck. Since data assembly and editing each family or volume is organized by different botanical gardens in different localities and latitudes, a well formulated working system is critical for a group of botanists, experts and gardeners from different gardens to work together and share information and build up a cordial and harmonious atmosphere that means failure or success for each volume of large families or genera. So far even after trials of the first two volumes, there are still many coordination issues to be solved and the Flora editing headquarter office also needs to be enhanced for coordination across many different gardens. For example, either morphological or phenological variation of individuals of same species or many other issues arise during data assembly and editing process, so that a harmonious working group is essential.

Fourth, taxonomic conflicts between Flora Reipublicae Popularis Sinicae and Flora of China have to be addressed. Even in the beginning of the Ex situ Flora of China, a determination that each entry must have a correct plant name (Latin name and widely accepted Chinese name) was formulated. However, there are many different treatments and name difference between Flora Reipublicae Popularis Sinicae and later updated English version Flora of China. Additional research is definitely needed in these situations although taxonomic research has not been prioritized in Ex situ Flora of China project because Editorial committee encouraged the Ex situ Flora of China to prioritize ex situ inventory and data collection as distinct from a traditional Flora based on herbarium specimens and less emphases on traditional Flora details such as, accepted name + literature cited, basionym + literature cited, synonym + year, type specimens, etc. This is true when many botanical garden staff involving the Ex situ Flora of China, highlight plant characteristics of ex situ collection without strong expertise in detailed taxonomic research. However, in cases of conflicts raised between names of Flora Reipublicae Popularis Sinicae and those of Flora of China, taxonomic research must be carried out without any choice. Coordinating taxonomic research between experts of living collections and taxonomist of herbaria is obviously a great challenge.

Nevertheless, since the project was initiated in 2012, significant progress has been made and many difficulties experienced and lessons learned. The Ex situ Flora of China is the first integrative ex situ Flora and will greatly benefit global ex situ conservation and provide needed basic and mega information services to agriculture, forestry, horticulture and medicinal industries in future.

Acknowledgments

The work is supported in part by China National Science and Technology Infrastructure Program 2015FY210100.

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