International Biological Flora: Ginkgo biloba

Abstract

en

1. This account presents information on all aspects of the biology of Ginkgo biloba L. (Ginkgo, Maidenhair tree) that are relevant to understanding its ecological characteristics. The main topics are presented within the standard framework of the International Biological Flora: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, reproductive and seed characters, herbivores and disease, history, conservation and global heterogeneity.
2. Globally, Ginkgo survives a wide range of mean annual temperature (−3.3 to 23.3°C) and annual precipitation (34–3925 mm) conditions, according to a meta-analysis. It prefers a warm, humid, open-canopy and a well-drained environment. The species shows strong tolerance to drought, freezing, fire, air pollution, heavy metals and low-level salt, whereas it is intolerant to long-time shade and waterlogging. Six Ginkgo trees even survived the atom bomb in Hiroshima, Japan, during World War II.
3. Ginkgo is susceptible to few diseases. Those occurring in nursery seedlings and juvenile trees involve stem rot and leaf blight. The former is caused by Macrophomina phaseoli, which could lead to a mortality rate of 5%–12% (up to 31.8%) for seedlings. This disease can be mitigated by a 4-h shading treatment and applying organic fertilisers. The pathogens inducing leaf blight include Alternaria alternata, Colletotrichum gloeosporioides and Pestalotia ginkgo, which may infect 100% juvenile trees in some regions. The application of 45% carbendazim or 50% Tuzet can effectively prevent leaf blight.
4. Ginkgo biloba is one of the world’s most distinctive trees with an important position in plant evolution and human society. It is a tall deciduous dioecious tree native to China. Refugial populations were identified in three glacial refugia located in eastern, southern and south-western China, respectively, with a patchy distribution pattern and a small population size. It typically grows along flood-disturbed streamsides in warm-temperate deciduous (and evergreen mixed) broadleaved forests. Ginkgo may have been introduced repeatedly out of China since the sixth century. It has been planted as a landscape tree world-wide, except in Antarctica. Ginkgo is also of great value for edible nuts, herbal medicine, religion and art. It is a natural and cultural symbol of China.

Abstract

zh

摘要

1. 本文系统总结了活化石树种银杏(Ginkgo biloba L.)的生物学和生态学特性。根据本刊“国际生物学植物志”的标准框架，我们从以下十一个方面进行了全面描述:分布、生境、群落、生物响应、环境响应、结构与生理、物候、繁殖和种子特征、植食动物与疾病、进化历史、保护、全球异质性。
2. 银杏具有突出的环境适应性和抗逆性。荟萃分析表明，银杏可适应变异范围极广的年均温(−3.3 至 23.3 °C)和年降水量(34至3925 mm)环境，但喜温暖、湿润、郁闭度低、排水状况良好的生境。银杏对干旱、霜冻、火、大气污染、重金属和低浓度的盐分具较强的耐受性，但不耐受长时间荫蔽和水淹。日本广岛市的六株银杏甚至经历第二次世界大战原子弹轰炸后仍存活至今。
3. 银杏也具很强的抗病性。大树病害极少，在幼苗和幼树中仅发现茎腐病和叶枯病。茎腐病由菜豆壳球孢(Macrophomina phaseoli)引起，幼苗致死率为5%–12%(最高达31.8%)，4小时遮荫处理外加施用有机肥可有效减轻症状。叶枯病的病原菌包括链格孢(Alternaria alternata)、盘长孢状刺盘孢(Colletotrichum gloeosporioides)和银杏盘多毛孢(Pestalotia ginkgo)。某些地区幼树的叶枯病发病率可达100%，但喷洒45%多菌灵或50%退菌特可有效预防叶枯病。
4. 作为全世界最独特的树种之一，银杏在植物进化和人类社会中扮演着重要角色。这种高大落叶乔木雌雄异株，原产中国，共有三处冰期避难所，分别位于华东、西南和华南。避难所种群分布零散，且种群大小较小。在暖温带落叶阔叶林和常绿落叶阔叶混交林中，常分布于沟谷两侧。自公元六世纪以来，银杏不断被引种至中国之外的世界各地，作为一种景观树种，目前银杏被栽培于除南极洲外的其余六大洲。它还具有很高的食用、药用、宗教和艺术价值。银杏是中国的自然和文化符号之一。

Ginkgo, or Maidenhair tree. Ginkgoaceae. Ginkgo biloba L. is a large deciduous tree. Crown conical initially, broadly ovoid when matured (Cheng & Fu, 1978). Branches nearly verticillate, ascending at about 45° from the trunk (Whetstone, 1993). Height normally 20 m (up to 70 m), trunk up to 500 cm wide in diameter (Xing, 2013). Bark light grey or greyish brown, longitudinally fissured especially on old trees. Long shoots pale brownish yellow when young, finally grey, internodes (1–) 1.5–4 cm. Short shoots blackish grey, with dense, irregularly elliptic leaf scars. Some branches of ginkgo are stalactite-like, known as ‘chichi’ (Li & Lin, 1991). ‘Chichi’ is developed from latent buds in trunks or roots (Del Tredici, 1992). Sometimes, ‘chichi’ can produce shoots and adventitious roots when cut off from the parent tree, as a way of vegetative propagation (Li & Lin, 1991). Winter buds yellowish brown, ovate. Leaves fascicled, with a (3–) 5–8 (−10) cm long petiole and a distinct notch which divides the leaves symmetrically into two halves (Cheng & Fu, 1978; Hara, 1997; van Beek, 2000). Leaves scatter on long shoots, or crowd at the apex of short shoots as a cluster, with 3–14 leaves (Cao, 2007). Blade flabellate, pale green, turning bright yellow in autumn, to 13 × 8 (−15) cm on young trees but usually 5–8 cm wide (Cheng & Fu, 1978). The leaf base is cuneate, slightly covered with brown hairs (Dörken, 2013).

Dioecious. Male cones ivory coloured, 1.2–2.2 cm long; pollen sacs boat shaped, with widely gaping slit. Ovules green and exposed to the air, 2–3 mm long, produced mostly in pairs at the ends of long peduncles, secretes a small droplet of mucilaginous fluid (pollination drop) from its apical tip (micropyle) which functions to capture airborne pollen. Only one (occasionally 2 or 3) ovule(s) can grow and develop to seed. Seeds elliptic, narrowly obovoid, ovoid or subglobose, 2.5–3.5 cm × 1.6–2.2 cm; sarcotesta yellow or orange-yellow glaucous, with rancid odour when ripe; sclerotesta white, with two or three longitudinal ridges; endotesta pale reddish brown. Pollination March to April, seed maturity September to October.

Ginkgo biloba is a relict species with an origin of 270 million years ago (mya) for its earliest ancestor, followed by a wide distribution across the world for diverse descendant species (Zhou et al., 2020). Ginkgo has only one extant species.

Ginkgo biloba is native to China while it has been commonly planted world-wide in university campuses, parks and gardens, or along streets and pavements. Old trees are common in temples, old villages or near streams in eastern Asia. Ginkgo is the cultural symbol of hope and peace in China and a popular candidate of the national tree. It is the city tree for a number of cities. Ginkgo leaf was designed as the logo of the XIX International Botanical Congress held in Shenzhen, China in 2017. Moreover, it is the logo of Botanical Society of China and several universities in eastern Asia, such as Zhejiang A&F University, the University of Tokyo and Osaka University.

1 GEOGRAPHICAL AND ALTITUDINAL DISTRIBUTION

It has long been controversial whether natural Ginkgo populations still exist. The long history of Ginkgo cultivation in China, together with the massive and intensive change of landscapes in China resulting from human activities, makes it extremely challenging to determine whether any truly natural populations remain (Crane, 2019). Some early researchers suggested that Ginkgo may have gone extinct in the wild (Chen, 1989; Sargent, 1916; Wang & Chen, 1983; Wilson, 1919; Wu et al., 1992; Zeng, 1935), while more scholars believed that natural Ginkgo can still be found somewhere, especially in Mt. Tianmu (Cheng et al., 1992; Del Tredici et al., 1992; Gong et al., 2008; Li, 1956; Li et al., 1981; Wang, 1961; Xiang et al., 2000; Zhao, 1997). Besides Mt. Tianmu and its adjacent mountainous regions in eastern China, Mt. Dahong in central China and Mt. Dalou (including Mt. Jinfo) in south-western China are highly likely homes to natural populations (Li et al., 1999; Shen et al., 2005; Tang et al., 2012; Xiang et al., 2001, 2006, 2007; Xiang & Xiang, 1999; Zhao et al., 2019).

Here, we recognise four regions where natural populations occur based on integrated lines of evidence: Eastern China, as represented by Mt. Tianmu, Zhejiang province; south-western China, as represented by Mt. Dalou (including Wuchuan county and Fenggang county), Guizhou province and Mt. Jinfo, Chongqing municipality; southern China, as represented by Nanxiong county, Guangdong province and Xing’an county, Guangxi province; central China, as represented by Mt. Shennongjia, Badong county and Anlu county, Hubei province, and Mt. Huping, Hunan province (Figure 1). The first three are Ginkgo refugia while central China harbours natural populations which are mixtures between south-western and southern populations as a result of range dynamics driven by climate oscillation c. 140,000 years ago (Zhao et al., 2019).

FIGURE 1

Distribution map of 11 evidenced natural populations of Ginkgo biloba. Four regions (including three refugia) are homes to these natural populations. The eastern China refugium (blue) is represented by Mt. Tianmu (TM), Zhejiang province. The south-western China refugium (red) is represented by Mt. Dalou including Wuchuan county (WC) and Fenggang county (FG), Guiyang city (GY) and Mt. Jinfo (JF). The southern China refugium (green) is represented by Xing’an county (XA, and Nanxiong county (NX). The central China (brown) is represented by Mt. Shennongjia (SNJ), Badong county (ES), Mt. Huping (HP) and Anlu county (AL). The map was retrieved from the International Scientific and Technical Data Mirror Site, Computer Network Information Center, Chinese Academy of Sciences (http://www.gscloud.cn/)

To acquire general distribution knowledge of world-wide Ginkgo, we queried the Global Biodiversity Information Facility (GBIF) database for out-China occurrence and China National Specimen Information Infrastructure (NSII) database for in-China occurrence as the first step. Then, a list of detailed locations for old Ginkgo trees in China (Xing, 2013) as well as long-term field surveys conducted by the Ginkgo research group at Zhejiang University (Lin et al., 2022) served as a complement. Moreover, a recent study provided us with more distribution information about Ginkgo plantations in China (Guo, Lu, et al., 2019). Finally, we generated a global distribution map of Ginkgo based on 10,918 records from herbarium specimens and field observations with accurate geographical coordinates. To ensure data precision and reduce data redundancy, we only included 5973 documented records with unique geo-reference for analyses.

Ginkgo is planted world-wide except in Antarctica (Figure 2), occupying a latitudinal range of nearly 103°. In the Northern Hemisphere, the highest latitude of its occurrence is 60°03′N in Europe. Most living Ginkgo trees are located in eastern Asia (mainly China, Japan and Korea; the CJK region hereafter), Europe and eastern North America (Figure 2). It has been planted in urban areas such as roadsides and parks for its attractive golden leaves in autumns. In eastern Asia, Ginkgo has a long plant history in the CJK region, where old trees frequently occur in the vicinity of temples and remote villages. In China, the latitudinal span of Ginkgo occurrence is nearly 25°, with the southernmost of 20°42′N and the northernmost of 45°32′N. Zhao et al. (2019) modelled its suitable present distribution range in China with occurrence records of sexually mature Ginkgo trees and 19 climatic variables. Their results showed that the overall distribution pattern of Ginkgo predicted for the present was largely consistent with its actual distribution. In Japan, Ginkgo can be found throughout all eight regions. Whereas in Korea, it has been planted massively across the country, particularly in coastal areas. The occurrence density of Ginkgo in India and North Korea may be underestimated due to the lack of precise geographical coordinates.

FIGURE 2

Global distribution map for cultivated and natural populations of Ginkgo biloba. The kernel density of Ginkgo’s occurrence was shown in the base layer. Zoomed panels represented 100 km × 100 km geographical grids (green) where Ginkgo trees mostly occur (North America, Europe and eastern Asia from the left to the right). Occurrence records (golden dots in zoomed panels) were compiled from GBIF database, NSII database, published literatures and long-term field survey results from Ginkgo research group in Zhejiang University

It has been believed that Ginkgo was initially introduced from Japan into Europe at the Botanic Garden in Utrecht, Netherlands in 1730 (Dallimore et al., 1966), followed by its spread in Europe. However, Zhao et al. (2019) revealed that the oldest trees in Europe were directly introduced from China rather than from Japan, followed by the introduction from Europe into North America. At present, Ginkgo is likely to be found in all temperate European countries, including 18 with known occurrence, that is the United Kingdom, Ireland, Norway, Sweden, Denmark, Poland, Germany, the Netherlands, Belgium, France, Spain, Portugal, Italy, Switzerland, Czech, Austria, Slovenia and Slovakia (Figure 2).

The first Ginkgo trees in the United States were introduced in 1784. They were first planted by William Hamilton on his estate, the Woodlands, Philadelphia, Pennsylvania (Del Tredici, 1981; Downing, 1841). Ginkgo now occurs in over 30 states (The Ginkgo Pages, 2021), and is common along the East Coast from New Hampshire to South Carolina as well as along the West Coast of Washington, Oregon and California (Figure 2). Also, Ginkgo trees have been sparsely planted in Canada, Mexico, Colombia, Chile, Bolivia, Brazil, South Africa, Russia, Iran, Kazakhstan, India, Australia and New Zealand (Figure 2).

The altitudinal range for Ginkgo is wide. It is mostly planted in lowlands of coastal and urban regions, while it occurs 300–1250 m above sea level (a.s.l.) in natural habitats of Mt. Tianmu (Lin et al., 2022; Xie, 2014) and 840–1200 m a.s.l. of Mt. Dalou (Tang et al., 2012).

2 HABITAT

2.1 Climatic and topographical limitations

Ginkgo is suited to the entire temperate and the Mediterranean range of climate (Zhou et al., 2020). Based on its world-wide occurrence and current climatic layers (1960–1990) from the WorldClim database (Hijmans et al., 2005), we assessed its climatic limits using the R package raster (Hijmans, 2019). Across its global distribution, Ginkgo shows tolerance to a wide range of temperature and precipitation conditions (Tables 1 and 2).

TABLE 1. Estimated temperature limitations of global Ginkgo biloba

Statistics values	Annual mean temperature (°C)	Mean diurnal temperature range (°C)	Isothermality (°C)	Temperature seasonality (°C)	Max temperature of warmest month (°C)	Min temperature of coldest month (°C)	Temperature annual range (°C)	Mean temperature of wettest quarter (°C)	Mean temperature of driest quarter (°C)	Mean temperature of warmest quarter (°C)	Mean temperature of coldest quarter (°C)
Min	−3.28	5.16	17.59	32.29	12.70	−26.00	10.00	−2.48	−16.60	6.07	−16.6
Mean	13.76	8.55	27.45	792.03	28.54	−1.80	30.34	20.79	5.43	23.27	3.77
Max	23.34	18.14	88.33	1546.47	41.30	12.90	54.60	28.72	26.73	32.18	18.08

• Note: Current temperature data were compiled from the WorldClim database with global occurrences of Ginkgo using the R package raster. Isothermality = (Mean diurnal temperature range/Temperature annual range) × 100; Temperature seasonality = standard deviation × 100.

TABLE 2. Estimated precipitation limitations of global Ginkgo biloba

Statistics values	Annual precipitation (mm)	Precipitation of wettest month (mm)	Precipitation of driest month (mm)	Precipitation seasonality (mm)	Precipitation of wettest quarter (mm)	Precipitation of driest quarter (mm)	Precipitation of warmest quarter (mm)	Precipitation of coldest quarter (mm)
Min	34	10	0	6	24	1	3	1
Mean	1097	185	31	57	477	111	437	127
Max	3925	684	149	152	1785	490	1785	632

• Note: Current precipitation layers were downloaded from the WorldClim database. Data were compiled based on global Ginkgo occurrences using the R package raster. Precipitation seasonality = coefficient of variation.

Species distribution modelling for Ginkgo in China suggested that its main climatic determinant was the mean temperature of the coldest quarter (Zhao et al., 2019). Local climatic conditions are substantially heterogeneous in the habitats harbouring natural populations. For example, in Mt. Tianmu, where Ginkgo trees grow from the foot (c. 300 m a.s.l.) to the vicinity of the peak (c. 1250 m a.s.l.), both the mean annual temperature and the mean temperature in January differ substantially along elevations (foot: 14.9 and 2.7°C vs near peak: 8.7 and −3.2°C) (Zhejiang Forestry Bureau, 1984). However, Ginkgo favours a moderate temperate climate in Europe. For example, the Ellenberg’s indicator value (Eiv) for temperature (T) corrected for Italy is 6 (Guarino et al., 2012).

Ginkgo prefers warm and humid weather rather than extremely low temperatures or strong winds (He et al., 1997). The mean annual temperature where Ginkgo is found is 13.8°C (Table 1) while that of temperate deciduous forests globally is 10°C (National Aeronautics and Space Administration, NASA). Ginkgo receives up to 3925 mm with an average of 1097 mm of rain per year (Table 2) while the average annual precipitation of global temperate deciduous forests is about 750–1500 mm (NASA). In its main areas in China, air humidity appears to be important in helping Ginkgo to survive. For example, the relative humidity of Ginkgo plantations in Changxing county (Zhejiang province), Taixing county (Jiangsu province) and Lingchuan county (Guangxi province) were 90%, 80% and 80% respectively (Cao, 2007). Chi et al. (2020) concluded that Ginkgo trees older than 100 years in China were mainly distributed east of the Hu Huanyong line, where the climate is humid.

The current association with high humidity could be a relic of its evolutionary history. Ginkgo is one of the most representative species among several living fossil plants in the core area of the Sino-Japanese flora (Hu, 1980; Zhou & Momohara, 2005), namely the Metasequoia Flora, where the Asian monsoon played a vital role in its evolution (Chen et al., 2018). Sedimentological and palaeo-floral data suggested that Ginkgo was largely confined to disturbed streamside and levee environments with a consistent set of companion species throughout the late Cretaceous and the Cenozoic, supporting a strong ecological conservatism (Royer et al., 2003). Under global warming scenarios, predictions suggested that no dramatic range contraction would occur for either natural or planted Ginkgo populations in China (Guo, Lu, et al., 2019; Tang et al., 2018).

Ginkgo shows few topographical limitations as it can grow on steep slopes, in ravines, near exposed cliffs and on limestone outcrops (Del Tredici et al., 1992; Tang et al., 2012). The average slope of its habitats can reach 30° in one of the natural populations located in Fenggang county, Guizhou province (Xiang & Xiang, 2008). Our plot survey on Ginkgo forests in Mt. Tianmu recorded slopes ranging from 12° to 58° (Lin et al., 2022).

2.2 Substratum

The optimum soils for Ginkgo are generally deep, free-draining, fertile, sandy loams with a water-table less than 1 m deep (Cao, 2007). However, it can grow on various soils, including sand, silt and clay. Soils weathered from many sorts of rock can provide substrata. It can be found rooted in soils derived from granite, gneiss, limestone, shale, among others, depending on its locality (Cao, 2007). The Eiv for nitrogen (N) corrected for Italy is 2 (Guarino et al., 2012), which suggests that Ginkgo can live on infertile soils. It is tolerant to a range of soil acidity from pH 4.5 to 8.5, though a pH of 6.0–8.0 is preferred (Cao, 2007). The corrected Eiv for reaction (R) in Italy is 6 (Guarino et al., 2012), indicating an association with weakly acidic to weakly basic conditions and never on very acidic soils. Ginkgo is highly drought resistant but sensitive to waterlogging (He et al., 1997). The growth of Ginkgo is closely related to water-tables, as it shows poor tolerance of submergence. The corrected Eiv for moisture (U) in Italy is 6 (Guarino et al., 2012), indicating that Ginkgo does not favour high moisture soil conditions in Europe. Under drowning conditions, the seedlings grow poorly and would be likely to die after 1 week (Cao, 2007).

3 COMMUNITIES

Natural Ginkgo populations can be found in warm-temperate deciduous (and evergreen mixed) broadleaved forests with moist, deep, sandy soils and full sunlight (Xiang et al., 2000; Yang et al., 2011). In one of its refugia, Mt. Tianmu, Ginkgo is a component of coniferous and broadleaved mixed forest with a normal-like distribution of the size frequency (Xiang et al., 2000). The stratification of the stands could be distinguished as four layers with Cryptomeria japonica var. sinensis as the dominant component of the canopy layer. The plant community in which Ginkgo forests were embedded has undergone deflected succession promoted by human activities (Xiang et al., 2000). Historically, mass plantings by monks made C. japonica var. sinensis the dominant species and strengthened the role of its wild individuals in the community, accelerating succession. Eventually, the original constructive species from Fagaceae, Lauraceae or Magnoliaceae were replaced by C. fortunei (Xiang et al., 2000).

In Mt. Tianmu, Ginkgo was mostly found with C. japonica var. sinensis (37.0%) and Pseudolarix amabilis (5.5%) among 713 recorded tree individuals (for the complete list of companion species, see Table S1) (Xiang et al., 2000). According to a recent plot survey on Ginkgo forests there, it was mainly accompanied with Phoebe sheareri (14.8%), Lindera praecox (7.1%) and Torreya grandis (5.8%), among 833 trees of 109 associated species (Lin et al., 2022).

In another refugium, south-western China, Yang et al. (2011) investigated seven sites located at Mt. Jinfo (Chongqing), Fenggang county (Guizhou province) and Wuchuan county (Guizhou province), where remnant Ginkgo stands can be found as components of mixed coniferous and broadleaved forests. Deciduous trees accounted for the vast majority of the relative dominance, and Ginkgo was the top-dominant species at all stands. The stratification of the woody layer at the stands comprised three layers with Ginkgo as the dominant component of the canopy layer. The Ginkgo community was presumed to be a specifically topographic climax community type developing on unstable micro-landforms which were well-watered and well-drained (Yang et al., 2011). The size frequency of Ginkgo was of the inverse-J type, suggesting good regeneration of Ginkgo populations (Yang et al., 2011). Ginkgo was companied by 81 woody plants, including Cunninghamia lanceolata, Juglans mandshurica, Aphananthe aspera and others (see Table S2). According to a study in Mt. Dalou (spanning Wuchuan county and Fenggang county) using 12 established plots, three plant community types were classified as dominated by only one species (G. biloba), two species (G. biloba-Cupressus funebris) or five (namely G. biloba-Liquidambar formosana-Cyclobalanopsis glauca-Cunninghamia lanceolata-Taxus wallichiana var. chinensis) at the floristic similarity level of 77% (Tang et al., 2012). Within these three plant community types, Ginkgo lived with L. formosana, C. lanceolata, T. wallichiana var. chinensis, Lindera megaphylla, C. glauca, Cornus controversa, Choerospondias axillaris var. pubinervis, J. mandshurica, Celtis biondii, Quercus aliena, Cinnamomum wilsonii, Machilus nanmu, Triadica sebifera, Acer laevigatum and others (see Table S3), many of which have been found in Ginkgo-bearing fossil sites in south-western Japan from the Pliocene to the Pleistocene (Tang et al., 2012).

Today, most Ginkgo trees are planted as landscape trees world-wide (The Ginkgo Pages, 2021). Across the Northern Hemisphere, it is now one of the most widely planted street trees (Crane, 2013), particularly in Asia, where it is closely associated with eastern religions. For example, Ginkgo was incorporated in the indigenous religion of Shintoism in Japan. Many of the large Ginkgo trees of China, Japan and Korea are on the grounds of Buddhist temples or Shinto shrines (Crane, 2013, 2019). In China, great trees can be found around old villages. In the United States, Ginkgo is among the most common street trees in Manhattan (Crane, 2019). In Europe, it is common in parks, gardens, school campuses and other urban landscapes (Crane, 2013).

4 RESPONSE TO BIOTIC FACTORS

Natural Ginkgo trees show good competitive ability, which benefits from a great facility for vegetative reproduction (Tang et al., 2012; Yang et al., 2011). In seven studied sites of Ginkgo communities, the stems of Ginkgo far outnumbered its companion species, which may account for its dominance in the canopy layer and better regeneration (Yang et al., 2011). Most undisturbed Ginkgo forests are dominated by it (Tang et al., 2012; Yang et al., 2011). However, Ginkgo persists in dense mixed forests dominated by C. japonica var. sinensis in Mt. Tianmu which has resulted from human activities (Section 3) (Xiang et al., 2000). In urban areas, street Ginkgo trees with 10–20 cm diameter at breast height (DBH) clearly showed weaker competitive ability compared to camphor trees (Cinnamomum camphora) (Y. P. Zhao, personal observation).

Ginkgo shows strong tolerance to various anthropogenic stress factors. One extreme exemplar is its resistance to damage from an atomic bomb. Ginkgo managed to survive the fire caused by an atomic bomb on Hiroshima during World War II and fresh young buds burgeoned soon afterwards (Hori & Hori, 1997). Today, there are still six Ginkgo trees standing within a radius of c. 2 km (1130, 1370, 1420, 1650, 1780 and 2160 m) of the blast centre (The Ginkgo Pages, 2021).

Tempered pruning is important to its growth and seed production (Cao, 2007). Excessive branching within its canopy can intensify the light competition within crown, leading to poor growth or even the death of branches (Cao, 2007). Controlled by moderate soil water stress, stomatal conductance was significantly increased by pruning, laying mulch and daily irrigation in Ginkgo (Kagotani et al., 2016). Also, Ginkgo maintained better leaf water status under severe water stress compared to Prunus yedoensis, another important urban street tree in Japan (Kagotani et al., 2016).

5 RESPONSE TO ENVIRONMENT

5.1 Gregariousness

In its natural habitats, Ginkgo grows as isolated trees or small patches. In Xingshan county, Hubei province, 92 old Ginkgo trees were documented across the county (Zheng et al., 2010). Within a 200 m × 200 m plot, 16 well-grown Ginkgo trees were marked. The density of the seedlings (23 seedlings per m²) is much higher than that in Mt. Jinfo (6.3 seedlings per m²) and Mt. Tianmu (3.3 seedlings per m²). In Mt. Tianmu, 36 Ginkgo individuals and 677 companion trees were documented along a transect of 27 ha (Xiang et al., 2000). In Fenggang county, a natural Ginkgo forest with an approximate area of 2000 m² consists of 69 Ginkgo trees along with 104 companions (Xiang & Xiang, 2008). Field surveys showed that Ginkgo was the only dominant species with a relative dominance from 67.5% to 95.0% for six of seven studied sites in Mt. Dalou where wild populations occur (Yang et al., 2011). In Mt. Dalou, numerous seedlings and 102 established saplings (1–8 m high) were found in rock crevices in sunny sites (Tang et al., 2012). However, seedlings and saplings are rare in Mt. Tianmu (Del Tredici et al., 1992). On the contrary, sprouts are common in natural populations (Del Tredici et al., 1992; Tang et al., 2012; Yang et al., 2011; Zheng et al., 2010).

Ginkgo is variably gregarious in urban and rural areas depending on planting purposes and strategies. It can be planted in landscapes in various spatial formations including individually (solitary trees), lines (e.g. street trees or sideway trees) or groups (e.g. Ginkgo communities or forests) (Handa et al., 1997). Ginkgo is the most planted street tree in Japan, comprising 552,407 individuals (11.5% of total street trees) in 1991 (Ministry of Construction, Japan, 1994) and 5,700,000 individuals (8.4%) in 2009 (Kurihara et al., 2014). There are nearly 60,000 Ginkgo trees in the five boroughs of New York City (Crane, 2019). A nationwide survey of planted trees older than 100 years found them in 818 counties of 23 provinces in China with an average density of 0.11 ± 0.04 trees per km² (Chi et al., 2020).

5.2 Performance in various habitats

Ginkgo can normally grow to 35–40 m but exceptionally to 70 m with a DBH exceeding 5 m (Cheng & Fu, 1978; Hori et al., 1997; Xing, 2013). The largest Ginkgo in Mt. Tianmu was reported to have a DBH greater than 120 cm (Del Tredici, 1992). In Ginkgo refugia, the height of the canopy layer of Ginkgo forests reaches 38 m in south-western China, 20 m in southern China and 32 m in eastern China (Lin et al., 2022; Tang et al., 2012). However, introduced Ginkgo can grow much taller. The tallest tree was reported to be 70 m tall, located in Zhangjiajie city, Hunan province, China (Zhang et al., 1992), though the precision of this field observation remains to be verified. The tallest (60 m) and widest (5.22 m DBH) Ginkgo trees in Korea were reported in Gangwon-do and Chungcheongbuk-do respectively (Xing, 2013). In Japan, Ginkgo can grow to nearly 50 m high (Xing, 2013). The oldest Ginkgo outside Asia is the male tree (1.31 m DBH) located at De Oude Hortus, Utrecht, the Netherlands, which may have been planted between 1730 and 1750 and grafted with a female branch in 1830 (Xing, 2013). Another male tree in Geetbets, Belgium may be as old and is now the widest (1.58 m DBH) Ginkgo in Europe (The Ginkgo Pages, 2021; Xing, 2013). In the United States, the biggest Ginkgo was recorded from Hyde Park, New York, at 26 m tall and 1.65 m DBH, planted by Dr. David Hosack (Del Tredici, 1981; Xing, 2013). Although Ginkgo has often been described as a slow-growing tree, it exhibits growth rates of up to 30 cm in height per year for the first 30 growing years under favourable conditions (Del Tredici, 1989). The growth is rapid when young, but slows down towards maturity (Del Tredici, 1991). Liang (1993) reported that the growth rate reached its peak at the age of 30–40 years. For example, 40-year-old Ginkgo trees are about 12 m high with roughly 30 cm DBH in Jiangsu province, while a 90-year-old tree in Mt. Tianmu, Zhejiang province is about 20 m high with 35 cm DBH.

An array of factors can affect the growth performance of Ginkgo. First, the presence of destructive diseases can lead to rather high mortality rate (Santamour et al., 1983). Only 56% of 638 field-planted Ginkgo trees survived after 34–52 years in the Blandy Plantation, Virginia, USA, which was possibly caused by pests. Second, abundant rainfall during the fast-growing season of Ginkgo (April–July), but not the high air temperature, increased the average annual increment in Szczecin, north-western Poland (Cedro et al., 2011). Third, reasonable fertilisation application can strongly facilitate the growth of Ginkgo, applied as N: 400 g, P: 200 g and K: 90 g per tree (Guo et al., 2016). Moreover, Ginkgo trees planted on sunny slopes generally grow better than those on shady slopes (Cao, 2007). However, Ginkgo at the reproductive stage has the best photosynthetic efficiency at 30%–35% of natural irradiance (Wang, Sun, et al., 2014).

In urban settings, pavements inhibit photosynthesis of Ginkgo significantly and the inhibition is greater under drought (Wang et al., 2019). Compared to ash (Fraxinus chinensis), Ginkgo showed overall less tolerance to paving (Wang et al., 2019; Wang, Wang, et al., 2020).

Ginkgo shows tolerance to a suite of gaseous air pollutants, except for a sensitivity to simulated acid rain (Kim, 1987; Oh et al., 1983). It was tolerant to sulphur dioxide, nitrogen oxides and ozone while it was moderately sensitive to fluorides (Davis & Gerhold, 1976; Davis & Wilhour, 1976; Karnosky, 1978; Weinstein, 1977). An investigation on the degree of leaf damage resulting from air pollutants suggested that Ginkgo was more tolerant to air pollution than 15 other trees, namely Pinus koraiensis, Pinus rigida, Abies holophylla, Pinus densiflora, C. japonica, Chamaecyparis pisifera, Chamaecyparis obtusa, Juniperus chinensis, Quercus serrata, Betula platyphylla, Populus occidentalis, Populus euramericana, Prunus jedoensis, Populus alba × glandulos and Paulownia coreana (Oh et al., 1983). Ginkgo grown in heavy traffic areas had fivefold higher sulphur contents than those growing in traffic-free areas (1.81% vs 0.36%) (Kim & Lee, 1990), possibly due to exhaust gases from cars and other particulates. Also, it showed greater accumulation ability for sulphur than three other coniferous trees, namely P. densiflora, Pinus koraiensis and Picea abies (Kim & Lee, 1990). No significant degradation of cuticular waxes was found in Ginkgo leaves collected from busy traffic areas. Ginkgo showed the most severe leaf injury among the gymnosperms when sprayed with pH 2.0 acid rain (e.g. 100% in Ginkgo, 76% in Abies holophylla and 12% in Pinus thungergii respectively) (Oh, 1986). The strong sensitivity of Ginkgo to simulated acid rain compared to other gymnosperms was possibly due to its special characteristics of leaf anatomy. The leaf epidermis has relatively thin walls, and hypodermal sclerenchyma is absent. Unlike many conifers, the stomata of Ginkgo occur almost exclusively on the abaxial surfaces of the leaves (Esau, 1977; Meidner & Mansfield, 1968). In addition, the structure of the epicuticular wax and its chemical composition may also determine the sensitivity of Ginkgo to simulated acid rain (von Schmitt et al., 1987).

5.3 Effect of frost, drought, fire etc.

Ginkgo is relatively hardy against frost. Although a late spring freeze led to a full defoliation of planted Ginkgo in the Missouri Botanical Garden in 2007, a new set of leaves sprouted later. A modified method of propagation can improve frost resistance, increasing survival rate from 71.8% to 89.5%: Placing the peeled ends of cuttings in a nutrient solution at 8–12°C for 5 days, then applying a 0.3 direct current for 90 s every 1 h to the nutrient solution at 2–4°C, for another 6 days (Hu, 2017).

The Eiv for salinity (S) corrected for Italy is 0 (Guarino et al., 2012), showing its intolerance to salinity, at least in Italy. However, Ginkgo is listed as a tree relatively strongly tolerant of salinity in China (Cao, 1999b). Five cultivars investigated showed stable permeability of the cell membrane under low salinity (<0.3%). Considering leaf K⁺ and Na⁺ concentrations, chlorophyll content, water potential, proline content and superoxide dismutase (SOD) activity among other indicators, Ginkgo showed relative strong tolerance to salt (0.15%–0.25%) compared with six other tree species (Cao, 1999b).

Ginkgo is fire resistant (Handa et al., 1997), showing the second lowest overall flammability compared with nine deciduous tree species, namely Melia azedarach, Toona sinensis, Acer truncatum, C. axillaris, Amorpha fruticosa, Nyssa sinensis, Ailanthus altissima, Gleditsia sinensis and Pterocarya stenoptera. Resistance was inferred from measurements of branch moisture content, rate of water loss and combustion intensity, suggesting that Ginkgo can be used for fire protection (Ding et al., 2016). It exhibited relatively low ignitability, medium combustibility and medium fire sustainability among eight woody species, namely Ginkgo, Camellia oleifera, C. camphora, Cedrus deodara, Liriodendron chinense, Nandina domestica, Cinnamomum burmannii and Osmanthus fragrans, and ranked the second-most fire-resistant tree based on comprehensive investigations (Wang et al., 2015).

High temperature or low precipitation will increase the risk of leaf scorch (Liang, 2016). When leaf scorch occurs, the lamina turns yellow with petiole becoming dry and brittle (Liang, 2016). In August, leaf scorch was found in 92.3% of trees investigated along four streets in Lanzhou city, Gansu province (Wang, 2018). Etiolation is also strongly affected by environment. Zhang (1993) found that the incidence of etiolation was 84%–100% from 1988 to 1989 in Taixing county, Jiangsu province. Factors that contributed to the presence of this condition included shortage of nutrients, extreme soil pH and high concentration of aluminium (Jiang et al., 2002; Zhang, 1993).

6 STRUCTURE AND PHYSIOLOGY

6.1 Morphology

Ginkgo is a large deciduous tree (Cheng & Fu, 1978). Branching is monopodial. The crown is conical at the juvenile stage and broadly ovoid when mature (Cheng & Fu, 1978). The dense, white wood has straight grain and is mainly composed of tracheids, with a small amount of xylem parenchyma. The wood lacks strength and durability and has lower density (0.5 g/cm³) than that of many conifers (Fei et al., 2000). Unlike other conifers, Ginkgo wood has tracheids which are irregularly arranged (Cheng et al., 1992). The tracheids are 2180–5710 μm (mostly 3160–4880 μm) long with 25–48 μm tangential diameter (Jiang et al., 2010).

Ginkgo has a typical taproot system. Anatomically, the young root of Ginkgo is diarch, but older roots become tetrarch or hexarch (Soh et al., 1988). The taproot is extensively branched and penetrates deep into the soil. The range of the root system is about double (1.9–2.5 fold) the canopy (He et al., 1997; Men, 1986). For example, the radius of distribution of the root system is more than 37 m for a 1000-year-old Ginkgo with a 30 m height and a 40 m crown diameter (He et al., 1997). The roots can be 5 m deep when grown on loose soil with neutral pH, low water-table and 40–60% relative soil moisture content (Cao, 2007). However, the distribution of fine roots is relatively shallow (<1 m). The fine roots are mainly distributed in the soil layer shallower than 80 cm, especially between 20 and 70 cm, which accounts for 76.4% of the total root biomass and 81.1% of the total fine root biomass (Cao, 2007).Ginkgo buds are yellowish brown and ovate with bud scales, including two types of buds, namely purely vegetative and mixed ones containing both vegetative and reproductive buds (Cheng & Fu, 1978). Vegetative buds usually develop into branches and leaves during the vegetative growth stage while mixed buds develop into leaves and strobili on short shoots during the reproductive growth stage. In addition, all parts of the trunk bear latent buds. Hence, it harbours strong ability of rejuvenation and regeneration (Cao, 2007).

Ginkgo has two types of shoots, namely the long shoot and the short shoot (the dwarf or spur shoot) (Foster, 1938). The long shoots are characterised by elongated internodes and relatively small pith and cortex. The short shoots have many abbreviated internodes and comparatively large pith and cortical regions (Foster, 1938). The long shoots are responsible for building up the basic framework of the tree and generating new growing points while the short shoots produce the majority of leaves and all of the reproductive structures (van Beek, 2000). The elongation rate of the long shoots can reach 100 cm per year in contrast to 0.3 cm for the short shoots. The short shoot has a long life span and can maintain its fecundity for 10 (up to 30) years (Cao, 2007).

Some stalactite-like branches occur on old Ginkgo trees, known as ‘chichi’ in Japan and ‘zhongru’ in China (Del Tredici, 1997). These unusual woody growths were first described by Fujii (1895) who considered this phenomenon a ‘pathological formation’ that developed in association with embedded shoot buds. Anatomically, ‘chichi’s are developed in all Ginkgo seedlings as part of their normal ontogeny from buds located in the axils of the two cotyledons (Singh et al., 2008). Both aerial and basal ‘chichi’ possess the ability to produce vegetative shoots and adventitious roots when cut off from the parent trunk and planted upside down in soil (Li & Lin, 1991). The ontogenesis of basal ‘chichi’ is closely related to pathogenic and drought stress, which may be an adaptive strategy of Ginkgo in the face of harsh environments (Men et al., 2021). Vegetative regeneration by means of basal ‘chichi’ has not only contributed to the long-term persistence of Ginkgo in the forests of China but may also have played a role in the remarkable survival of the genus since the Cretaceous (Del Tredici, 1992).

Long-shoot leaves have a 2–5 cm petiole, whereas in short-shoot leaves it is only 1–4 cm (Dörken, 2013). The mean leaf area was 50.5 cm² on the long shoots and 28.3 cm² on the short shoots (Dörken, 2013). Occasionally, leaves can become variegated or tube shaped. Some Ginkgo cultivars can also develop ovules on the leaves and produce seeds (Cao, 2007).

Leaves are hypostomatous with stomata primarily on the abaxial (lower) leaf surface (Maácz, 1957). Occasionally, full-grown stomata have been observed on the adaxial surface (Kanis & Karstens, 1963; Kausik, 1974). The stomatal apparatus is the haplocheilic type and is distributed irregularly among veins. The average length of stomatal guard cells is 45.9–55.7 μm (Šmarda et al., 2018). Stomatal density ranges from c. 100 to 140 per mm² (Chen et al., 2001; Kanis & Karstens, 1963) and is sensitive to multiple environmental factors, including humidity, sunlight, sunshade and atmospheric CO₂ (Chen et al., 2001; Conde, 2016).

6.2 Mycorrhiza

Arbuscular mycorrhizal fungi (AMF) colonise the roots of Ginkgo (Fontana, 1985; Khan, 1970). These AMF mainly belong to Glomus and Gigaspora (Chen & Han, 1999). The occurrences of intracellular hyphae are abundant on Ginkgo roots while the intercellular hyphae were rarely found (Fontana, 1985). However, the intercellular hyphae were not observed from other gymnosperm species like Taxus baccata (Strulu, 1978), Sequoia gigantea or Sequoia sempervirens (Mejstrik & Kelley, 1979). This pattern implies that the endophytic fungi may penetrate from cell to cell in gymnosperms. Ectomycorrhiza has not been reported in Ginkgo.

AMF can significantly facilitate the growth of seedlings (Qi et al., 2002; Zhang, Qi, et al., 2002). AMF-inoculated Ginkgo seedlings performed better than the control in terms of seedling height (increased 33.3%–67.9%), dry weight of leaves (increased 15.3%–53.6%), leaf area (increased 10.8%–23.7%) and leaf dry weight (increased 14.4%–33.2%) (Zhang, Qi, et al., 2002).

6.3 Perennation: reproduction

Phanerophyte. Reproduction is primarily by seeds. Ginkgo has a long juvenile period and strobili are first produced at approximately 20–30 years of age (Del Tredici, 2007; Hadfield, 1960). It has a long life span, as the oldest Chinese individual located in Mt. Fulai, Shandong province was reported to be more than 3000 years old (planted in the Shang Dynasty) (Hori et al., 1997; Sun, 1982). Strikingly close similarities were observed between the young trees (20 years) and the old trees (600 years) in terms of leaf areas, leaf photosynthetic efficiencies or seed germination rates (Wang, Cui, et al., 2020).

Naturally, Ginkgo can produce numerous sprouts, suckers or air roots from the roots and branches when the above-ground part is damaged (Del Tredici, 2001; Tang et al., 2012), which provides it with outstanding regeneration potential. Layered sprouts arising from low-hanging lateral branches can produce adventitious roots where they reach the soil. Eventually, these branches form vertical shoots that can develop into autonomous trunks when the parent branch rots away (Del Tredici, 2001). In addition, ‘chichi’ can also produce numerous vegetative shoots (Del Tredici, 1992). The most striking feature of Ginkgo in Mt. Tianmu was the multi-stemmed form of large old trees which may be related to the presence of ‘chichi’ (Del Tredici, 1992).

Ginkgo can be reproduced asexually through both hardwood and softwood cuttings. Hardwood cuttings are best collected from 1- to 3-year-old branches on trees younger than 30 years in early winter, while the ideal materials for softwood cuttings are 1-year branches from 2- to 15-year-old trees in spring and summer (Cao, 2007). The survival rate of cuttings can be increased by the treatment with rooting powder which contains indole-3-acetic acid (IAA) and naphthalene acetic acid (NAA) (Li & Cao, 2004; Tan et al., 2000).

Ginkgo can be grafted onto rootstocks in different seasons in various ways, such as cleft grafting, bark grafting, splice grafting, whip and tongue grafting (Cao, 2007). The survival rate can reach 91% by cleft grafting during July and August (Zhuang et al., 1987). Cleft grafting and splice grafting were widely used in northern China plantations with survival rates up to 88% (Lu, 1986).

Organ culture, pollen culture and somatic embryogenesis are applicable for Ginkgo propagation, but require appropriate conditions and approaches (Chen & Cao, 2006; Guo, 2004). For organ culture, stem segments are mostly used as initial materials. For pollen culture, the application of IAA is recommended to ensure the development of embryos (Laurain et al., 1996). During the somatic embryogenesis process, embryos can develop into cotyledons but no seedling will form eventually (Hao et al., 2000; Wu & Yan, 1998).

6.4 Chromosomes

Ginkgo is diploid with 2n = 24 chromosomes (Ishikawa, 1910; Newcomer, 1954; Pollock, 1957; Tanaka et al., 1952). Polyploid and haploid have been observed in cultivated Ginkgo (Šmarda et al., 2016, 2018), although no polyploid was found in a wild population (Y. P. Zhao, personal observation). A flow cytometry survey in European Ginkgo collections and their seedlings (>2200 individuals of c. 200 cultivars) revealed ploidy variation with 13 haploid, three triploid and 10 tetraploid trees, most of which also differed from diploids in morphology of leaves and stomata (Šmarda et al., 2018). The mean absolute length of chromosomes is 7.6 μm (6.4–9.3 μm) with the mean length of 5.4 and 2.2 μm for long and short arms respectively (Xiang et al., 2007).

The genome size of Ginkgo (11.8 ± 0.4 pg, 1C; Zonneveld, 2012) is large compared to that of angiosperms but relatively small for gymnosperms (average C value: 18.1 pg, 17.7 Gb; Hamilton & Buell, 2014). The first draft genome of Ginkgo was assembled with a size of 10.6 GB which included 76.6% repetitive sequences (Guan et al., 2016). A new version of the genome, using both the short and long sequencing reads, is 9.9 Gb in size (Liu et al., 2021).

Sex chromosomes of Ginkgo were first reported in 1954 (Lee, 1954; Newcomer, 1954), while its sex determination system was confirmed as male heterogamety (XX/XY), based on resequenced genome data from 97 males and 265 females (Zhang, Zhang, et al., 2019). A 4.2 Mb sex determination region (SDR) was identified on the X chromosome, which may contain three evolutionary strata. A longer SDR (17 Mb) has also been reported (Liao et al., 2020).

6.5 Physiological data

Generally, Ginkgo prefers sunny conditions. The Eiv of Ginkgo for light condition (L) corrected for Italy is 7, same as those of Cupressaceae species (Guarino et al., 2012). Though Ginkgo trees are mostly planted in open areas with full light, it withstands shade to a certain extent in natural populations. The light saturation point of Ginkgo is about 1000–1200 μmol m⁻² s⁻¹, which is similar to Cycas species (Jiang & Xu, 2006; Tang et al., 2020; Zhang, Cao, et al., 2002). However, seedlings have a strong tolerance to shade (Sarijeva et al., 2007). Under long-term shading conditions, the content of chlorophyll in leaves increased significantly (Lichtenthaler et al., 2007; Sarijeva et al., 2007; Zhang, Cao, et al., 2002). The photosynthetic decline caused by shading was relatively weak (Zhang, Cao, et al., 2002). When the light flux reached 1500 μmol m⁻² s⁻¹, a higher proportion of absorbed light energy was dissipated as thermal to protect against photodamage (Sarijeva et al., 2007; Zhang, Cao, et al., 2002). Specific leaf area (SLA) is a useful measure of leaf economy and represents one main axis of the plant ecology strategy scheme (Westoby, 1998). Among 642 measured leaves from the Ginkgo canopy, the SLA varied from 36.7 to 225.6 cm²/g, an approximately sixfold range (Christianson & Niklas, 2011). The average value of SLA differed between long and short shoots (94.3 vs 131.8 cm²/g), between the male and female (85.8 vs 146.5 cm²/g), and between the short shoots with or without of seeds (148.3 vs 115.4 cm²/g) (Christianson & Niklas, 2011). Compared to 45 other studied gymnosperms, Ginkgo had a greater value of SLA on average (134.5 vs 64.1 cm²/g) (Paź-Dyderska et al., 2020).

Ginkgo shows strong tolerance to drought (Cao, 1999b), which may be a benefit from its well-developed root system. After 24 h of exposure to 15% polyethylene glycol (PEG), the membrane permeability of Ginkgo increased to 19.2%, which was roughly 1.5-fold the control, indicating that the protoplasm has strong resistance to dehydration. After 48 h of exposure to 15% PEG, the root vitality decreased significantly (63.8% of the control), but nearly recovered to the control level (98.8%) within 2 days (Cao, 2007). Among seven afforestation tree species, Ginkgo showed second-best drought resistance, only inferior to Pinus massoniana (Cao, 1999b). It still grows well in Taiyuan city, Shanxi province, with an annual precipitation of no more than 500 mm (Cao, 2007). During 2010–2012, when midsummers were unusually hot (2.4–2.8°C higher maximum temperature than the long-term mean) and dry (6%–56% precipitation of the mean) in Japan, Ginkgo showed higher stomatal conductance and midday leaf water, suggesting that it had higher drought resistance than the other two common street trees, namely Prunus × yedoensis and Zelkova serrata, and was less susceptible to urban street conditions (Osone et al., 2014). Ginkgo can grow normally under mild water stress (−0.3 MPa water potential), but cannot survive longer than 18 days under strong water stress (−2.0 MPa) (Chen et al., 2002). Also, the adaptability of Ginkgo to drought stress was found to be sex biased; female individuals showed overall better growth and physiological activity than males under strong drought treatment (He et al., 2016).

Physiological behaviour of Ginkgo can be strongly affected by heavy metal stress (Cao, 2007). Under the joint stress of cadmium (Cd) (150 mg/kg) and lead (Pb) (1000 mg/kg) with 30 days of exposure, the ultrastructure of leaves disintegrated (Zhu et al., 2006). In the root system, the ion homeostasis was also distorted due to the inhibition of Mg²⁺ absorption. However, calcium and potassium ion homeostasis were maintained, suggesting resistance to heavy metal stress (Zhu et al., 2006).

6.6 Biochemical data

Ginkgo contains various types of bioactive compounds, of which flavonoids and terpene trilactones were determined to be the majority (Singh et al., 2008). More than 40 flavonoids were identified from the leaves (Furukawa, 1932, 1933; Joly et al., 1980). Common flavonoids include anthocyanins, flavanols, flavones and proanthocyanidins (PAs), many of which were considered to function against biotic and abiotic stresses (Ma et al., 2018). For example, flavanols protect plants from ultraviolet (UV) damage and anthocyanins function as signals for insects, while PAs act as herbivore deterrents and antimicrobial compounds (Barbehenn & Constabel, 2011; Gould, 2004; Treutter, 2006). Other important leaf secondary metabolites are terpenoids like ginkgolides and bilobalide, which can only be found in Ginkgo (Sun et al., 2020). Terpenoids are synthesised in Ginkgo roots and then transported to the leaves through the stem cortex and phloem (Cartayrade et al., 1997; Lu et al., 2017; Neau et al., 1997). According to hydroxyl positions, ginkgolides can be mainly divided into seven types (ginkgolide A, B, C, J, K, L and M), among which ginkgolide B (GB) showed the highest activity (Li et al., 2020). The content of each flavonoid and terpenoid varies with season (Cao, 2007). Terpenoid content was relatively low in spring, but gradually increased and reached the highest level in late summer and early autumn (c. 0.23%) (Leng et al., 2001; van Beek & Lelyveld, 1992). In contrary findings, the content of flavonoids was high in April, with 2.75% in juvenile leaves and 0.81% in mature leaves, while lowest in late summer, with 1.04% in juvenile leaves and 0.47% in mature leaves (He et al., 1998).

Temperature, precipitation and soil moisture can all affect the biosynthesis and accumulation of flavonoids in leaves (Wang et al., 2015; Wang, Cao, et al., 2014). For 2-year-old seedlings, flavonoid accumulation was significantly greater under lower temperature (15°C day and 5°C night) and lower available soil moisture (40%–45% and 30%–35% of field capacity) while it was strongly suppressed under high temperature (35°C day and 25°C night) (Wang et al., 2015). It was found that higher elevation, lower temperature, stronger UV-B and light flux generally facilitate flavonoid synthesis (Guo et al., 2020; Xu, Wang, et al., 2014; Zhao et al., 2020; Zou et al., 2019). In China, concentrations of secondary metabolites (such as isorhamnetin) in the leaves from 10 populations differed significantly, which may be associated with altitude and annual rainfall differences (Zhou et al., 2017). Moreover, studies showed that physiological etiolation can reduce the activity of peroxidase (POD), phenylalanine ammonia-lyase (PAL) and polyphenol oxidase (PPO) (Wang, 2008).

Seed kernels contain about 38.2% carbohydrate, 6.9% protein, 2.4% lipids and 58% water, with a few alkylphenol compounds at maturity (Cao, 2007). Kernels are also rich in metallic elements (Fe, 13.0–26.8 mg/g; Zn, 10.0–20.5 mg/g; and Cu, 4.0–10.7 mg/g) (Lin et al., 2002). In addition, kernels contain toxic substances, mainly 4′-O-methyl pyridoxine, which causes paroxysmal spasms (Kobayashi et al., 2011). The sarcotesta contains two volatile compounds, butanoic and hexanoic acids (Hori et al., 1997), which account for its unpleasant odour when rotting. The seeds also contain phenolic compounds which can cause human contact dermatitis (Hori et al., 1997).

Pollen contains about 27% protein whose content of different amino acids varies, with the richest being aspartic acid (3.11%) (Cao, 2007; Zhao et al., 1997). Pollen is also rich in flavonoids, but with hardly any terpenoids (Bao et al., 1999). In particular, the vitamin E content of pollen can reach 30 g/kg, which is nearly twice of that in P. densiflora (17.4 g/kg) and Zea mays (15.4 g/kg) (Cao, 2007; Sun et al., 2006).

Leaves can emit volatile compounds, including alkanes, aldehydes, alkenes, aromatic compounds, esters, terpenes and ketones (Li et al., 2011). The emission rate of volatile compounds can be affected by season, light condition and temperature (Li et al., 2011).

7 PHENOLOGY

Vegetative buds generally open in March (Cao, 2011), but northern populations can delay opening until April (Cao, 2011; Xu, Xu, et al., 2014). In Liaoning province, China, leaf emergence began on 13 April (±9 days) (Xu, Xu, et al., 2014). In Japan, the average day of leaf budburst (c. 20% of all leaf buds are open) was on 12 April (Doi et al., 2010), and budbreak occurs 40 days earlier in the south (30°N) than that in the north (43°N) (Del Tredici, 2007). Winter chilling is a determinant in foliar budbreak (Wilson et al., 2003). Under 3 consecutive years of the same treatments, Ginkgo trees required a minimum of 100 chill hours (maintained at 3°C) plus 936 greenhouse hours (maintained above 22°C) to initiate budbreak, and a minimum of 500 chill hours plus 1168 greenhouse hours to reach 50% budbreak (Wilson et al., 2003). The sensitivity of leaf unfolding to warming was higher (4.17 days °C^-1) and the photoperiod effect was larger (decreased by 1.15 days °C^-1) at the lower elevation (344 m) than at the higher elevations (1098 m) (Wu et al., 2022).

Males seem to bloom earlier in spring earlier than females, which may result from a higher heat requirement for leaf unfolding in females (Wu et al., 2022). The male mixed buds begin to open in early March while in northern populations it is often delayed to mid-April (Lu et al., 2011; Wang et al., 2013). After a week, the green male cones tend to droop, perpendicular to the fan-shaped leaves above (Lu et al., 2011). By mid-April, the main axis elongates and separates the microsporophylls, then male cones turn yellow and begin to shed pollen (Lu et al., 2011). A large amount of pollen grains disperse within 7 days (Gao et al., 2001; Lu et al., 2011). The female mixed bud scales begin to unfold in late March. The bud scales continuously unfold, resulting in the appearance of the leaves and ovules (Jin, Wang, et al., 2012). In mid-April, a pollination drop appears on each micropyle, signalling that the ovule is well-prepared both morphologically and structurally for pollen entrapment (Cao, 2007; Jin, Wang, et al., 2012).

Seed abscission begins in mid-August to late September, about 140–190 days after fertilisation (Cao, 2011; Feng et al., 2018). Seeds mature during September to October (Cheng & Fu, 1978) and after-ripening lasts until late November (Cao, 2011). Leaf colouring usually begins at the end of September or October (Cao, 2011; Doi & Takahashi, 2008). Leaf abscission begins from late September to late November and lasts for about 16 days in northern China and Japan (Cao, 2011; Doi & Takahashi, 2008; Xu, Xu, et al., 2014).

8 REPRODUCTIVE AND SEED CHARACTERS

8.1 Reproductive biology

Ginkgo is a dioecious species with a remarkably long juvenile period. Sexual maturity is reached at 20–30 years old (Singh et al., 2008). Many reports suggested that female trees were more common than male ones in natural populations (Shang et al., 2007; Sun et al., 2015; Xiang et al., 2001; Xiang et al., 2003). However, a few natural populations were male biased, such as those in Wuchuan county, Guizhou province (♂:♀ = 1.4:1) (Xiang & Xiang, 1997) and Mt. Tianmu (♂:♀ = 1.2:1; Lin et al., 2022). Santamour et al. (1983) noted that the sex ratio was roughly 1:1 at the Blandy Experimental Farm in Boyce, Virginia. Most Ginkgo populations at nurseries in China were reported to be male biased (55%–70%; Guo, 1993).

Male cones are borne in the axils of bracts on the short shoots (Del Tredici, 2007; Mundry & Stützel, 2004). Mature male cones are pendulous and catkin like (Mundry & Stützel, 2004). Three to seven male cones tuft at the tip of short shoot (Lu et al., 2011). A mature male cone is ivory coloured, 1.2–2.2 cm (2.4 ± 0.3 cm) long and 0.5 ± 0.2 cm wide, and contains 60–80 microsporophylls spirally arranged around the main axis (Cheng & Fu, 1978; Lu et al., 2011). A microsporophyll is usually composed of a sterile extension and two elliptical microsporangia about 2.8 ± 0.5 mm long and 1.1 ± 0.1 mm wide (Lu et al., 2011). The pollen is boat shaped, 12.1 ± 1.3 μm in polar view and 33.7 ± 1.7 μm in equatorial view, during dispersal. It has a large aperture area and three pollen wall layers with (Lu et al., 2016).

Generally, two ovules are held partially erect on opposite sides of the ovulate peduncle on female short shoots of Ginkgo (Jin, Zhang, et al., 2012). A mature ovule is 2–3 mm long (Cheng & Fu, 1978). Each ovule differentiates into the integument, nucellus and collar (Douglas et al., 2007). The collar is the upper lateral portion of the axis, proximal to the ovule, knob-like and enlarged, with numerous stomatal pores and a large number of mucilaginous ducts and crystals (Carothers, 1907; Douglas et al., 2007).

Ginkgo is a typically anemophilous plant, that is pollinated by wind, like most gymnosperms (Niklas, 1985). A mature male tree can produce 12,000–17,000 pollen grains per year (Xing et al., 1998). Mature pollen is shed from microsporangia and floats in the air until it is trapped by the pollination drop which can transport pollen to the nucellar surface (Cheng et al., 2018; Jin, Jiang, et al., 2012; Jin, Wang, et al., 2012). Once inside the ovule, the male gametophyte commences a 4-month long development period that culminates in the production of a pair of multi-flagellated spermatozoids, one of which fertilises a waiting egg cell (Friedman, 1987). After pollination, the colour of ovules changes from yellow to green as the pollination drop disappears (Jin, Wang, et al., 2012). Usually, only one ovule grows and develops into seed on each ovulate peduncle, although two or three ovules can grow seed occasionally (Cheng & Fu, 1978). The mean distance of pollen dispersal was reported 852 m with a maximum range of 20 km in Mt. Tianmu (Xie, 2014).

8.2 Hybrids

Ginkgo is the only extant species in Ginkgo L., with all its close relatives being extinct (Zhou et al., 2020). Thus, no hybridisation events have been observed between Ginkgo and any other species.

8.3 Seed production and dispersal

The mature seed is large (25–35 mm × 16–22 mm), elliptic, narrowly obovoid, ovoid or subglobose (Cheng & Fu, 1978). Mature seeds are composed of a fleshy sarcotesta (orange-yellow and glaucous), a hard and stony sarcoderm (white, with two or three longitudinal ridges), a membranous endopleura (reddish brown) and an embryo surrounded by female gametophyte (Holt & Rothwell, 1997). When shed from the parent sporophyte, the seed is covered with the fleshy sarcotesta which finally disappears several months later (Holt & Rothwell, 1997). The mean seed fresh weight was 10.1 g in the middle of September, with 64.3% water content (Feng et al., 2018). In December, the mass of each seed decreased to 7.6 g, reaching minimum size (about three fifths of its volume in September) (Feng et al., 2018). A seed excluding the fleshy sarcotesta is referred to as the Ginkgo ‘nut’ with a size of 19–30 mm × 11–14 mm (Del Tredici, 1989). The Ginkgo nut mainly constitutes endosperm, while the embryo accounts for no more than 1% of the seed volume (Feng et al., 2018).

The full seed yield period starts at about 40 years old or older; it can be extended to 150–200 years (He et al., 1997). It was reported that 700,000–800,000 trees can produce an average of 6000–7000 t of dry nuts per year (Singh et al., 2008). However, the annual productivity of seeds varies among producing areas and individual ages. In Suzhou city, Jiangsu province, a 130-year-old Ginkgo produces 150–250 kg seeds per year. A 500-year-old tree in Taixing county, Jiangsu province yields 25–50 kg of seeds per year. In Xingshan county, Hubei province, one healthy mature tree can produce c. 200 kg seeds per year on average (up to 400 kg) (Zheng et al., 2010). The maximum yield record for a single tree is 600 kg, corresponding to about 2 kg seeds per m² of the projected area of the tree crown (He et al., 1997). The commercial industry of Ginkgo nuts has been developing for more than 600 years in China. About 44 cultivars have been selectively bred based on quality, size and productivity of their nuts (Singh et al., 2008). For example, Dafushon, a widely grown cultivar, can produce 50–100 kg from a 50-year-old tree in Jiangsu Province, China (Singh et al., 2008).

Seeds are primarily dispersed by gravity followed by secondary dispersal (Xie, 2014). The mean dispersal distance of a seed is 462 m (450–474 m) in Mt. Tianmu based on a parentage analysis and water-mediated dispersal along the stream may not play a role (Xie, 2014). A number of extant animals are reported to feed on and presumably help disperse the seeds of Ginkgo. In China, dispersal agents include two members of the order Carnivora, the leopard cat (Felis bengalensis) recorded in Hubei province (Jiang et al., 1990) and the masked palm civet (Paguma larvata) recorded in Zhejiang province (Del Tredici et al., 1992). Another member of the Carnivora in Japan, the raccoon dog (Nyctereutes procyonoides), was also documented to feed on Ginkgo seeds (Rothwell & Holt, 1997). Beech marten (Martes foina) also eats Ginkgo seeds at the campus of Heidelberg University, Germany (Y. P. Zhao, personal observation). Multiple transitions of seed dispersers may have occurred along geological time. A long-tailed bird (Jeholornis sp.) from the Early Cretaceous in China might have facilitated seed dispersal of Ginkgo, as its fossil contains a large number of Ginkgo-like seeds in its crop (Zhou & Zhang, 2002). The extinct mammalian multituberculate (Ptilodus kummae) might be the dispersal agent in the Palaeocene and the Eocene (Del Tredici, 1989).

8.4 Viability of seeds: germination

Ginkgo seeds require an after-ripening period of 40–50 days for the physiological maturation of the embryo (Cao & Cai, 2006). The underdeveloped status of the embryo at the time of abscission accounts for such germination delay (Li, 1934; Li & Chen, 1934). Cold stratification of seeds is not a strict prerequisite for germination but can increase overall germination percentage and accelerate the progress of germination (Del Tredici, 1991; Holt & Rothwell, 1997; Johnson & Wickliff, 1974; West et al., 1970). The length of the embryo increased from 0.6 to 1.3 cm after 5 months of 2–5°C cold stratification (Cao & Cai, 2006). Soaking seeds in water at 30°C for 2–4 days can effectively shorten the dormancy breaking period to 15–20 days with germination above 85% (Cao, 2007). Germination generally increased with higher temperatures (82.6% at 25°C and 84.8% at 30°C) but decreased to 73.7% at 35°C due to seed rotting (Feng et al., 2018). Also, proper pre-sowing treatments can strengthen the growth vigour of stratified Ginkgo seeds. After being stored at 4 ± 1°C for 60 days, the germination rate increased from 28.5% to 80.9% and the height and biomass of seedlings significantly increased (Sofi et al., 2018). Moreover, Johnson and Wickliff (1974) reported that exposure to red light also accelerated the germination rate of intact, unstratified seeds.

Dormancy is regulated by hormones (Cao & Cai, 2001). The level of gibberellic acid (GA) was approximately 100-fold greater in stratified embryos versus unstratified ones (West et al., 1970). The ratio of GA to abscisic acid (ABA) increased from 1.1 to 5.5 after 3-month stratification treatment (Cao & Cai, 2006). In addition, the kernel contains a large amount of amygdalin, a cyanogenic glycoside, which has a strong inhibitory effect through releasing HCN in wet environments (Cao & Cai, 2001).

Numerous seedlings and 102 established saplings were recorded in the sun-exposed habitats of rock crevices for the natural population in south-western China (Tang et al., 2012). On the contrary, seedlings and saplings are almost absent for the other natural population in Mt. Tianmu of eastern China (Del Tredici, 1992). However, our field survey showed that seedlings are relatively rich in a sun-exposed habitat in Mt. Tianmu, indicating that light might be crucial for seed germination (Y. P. Zhao, personal observation).

8.5 Seedling morphology

Germination is hypogeal and usually is complete (when the first true leaf appears) after 4–5 weeks (Soma, 1997). Seedling morphology is shown in Figure 3.

FIGURE 3

Seedlings of Ginkgo biloba at (a) 1 week, (b) 2 weeks, (c) 3 weeks, (d) 4 weeks, (e) 5 weeks and (f) 9 weeks after germination. Illustration was drawn by Ruo-Yu Xu

9 HERBIVORY AND DISEASE

Generally, Ginkgo is highly resistant to insect feeders and pathogens like fungi, viruses and bacteria (Del Tredici, 1991; Major, 1967). Chemical defences against herbivorous insects may be one of the reasons why Ginkgo survives as a living fossil (Honda, 1997). Nevertheless, some invertebrates can cause serious damage. Fungal diseases like stem rot and leaf spot can also cause great damage.

9.1 Animal feeders or parasites

Vertebrate feeders that also disperse Ginkgo seeds are described in Section 8.3. Modern tree squirrels in the genus Sciurus (Rodentia, Sciuridae) (Del Tredici, 2007) also eat them.

Invertebrates associated with Ginkgo are listed in Table 3. Studies suggest that Ginkgo is less infected by insects than other trees (Kawai, 1977; Yu et al., 2014). For example, among the 344 insects found in 40 landscape trees in Japan, only six could infest Ginkgo (Kawai, 1977). In China, the numbers of recorded insects feeding on Ginkgo varied across regions (Gu et al., 2012; Huang, 1994; Leng et al., 2014; Wang et al., 2011, 2016; Zhou et al., 2013). Up to 65 insect feeders were found in northern Guangxi province (Huang, 1994) while only eight underground pests were listed in research conducted in Linyi city, Shandong province (Leng et al., 2014). According to a 20-year investigation in eastern China, the documented underground insect feeders are mainly beetles, while Pammene ginkgoicola Liu (Lepidoptera, Tortricidae) is the predominant branch miner (Wang et al., 2016). The yellow tea thrip (Scirtothrips dorsalis) causes the greatest damage to Ginkgo leaves among sucking insects while Lepidoptera and Coleoptera are predominant defoliators (Wang et al., 2016).

TABLE 3. Invertebrates recorded from Ginkgo biloba world-wide. Nomenclature follows that of the Database of Global Biodiversity Information Facility (GBIF, 2020) or Database of European or Mediterranean Plant Protection Organization (EPPO, 2020)

Species/classification	Ecological notes	Source
Arachnoidea
Tarsonemidae
Polyphagotarsonemus latus (Banks)		1
Blattodea
Rhinotermitidae
Coptotermes communis (Xia et He)		1
Coptotermes formosanus (Shiraki)	Stems	1
Reticulitermes chinensis (Snyder)		1
Reticulitermes speratus (Kolbe)		1
Termitidae
Macrotermes barneyi (Light)		1
Coleoptera
Cerambycidae
Acalolepta gingovora (Makihara)	Live bark	2
Acalolepta sejuncta (Bates)	Twig	2
Anoplophora chinensis (Forster)	Larvae; stems; variety of trees	1
Anoplophora glabripennis (Motschulsky)	Larvae; stems; variety of trees	1
Trirachys orientalis (Hope)		1
Curculionidae
Hypomeces squamosus (Fabricius)	Bud, leaves	1
Sympiezomias velatus (Chevrolat)	Bud, leaves	1
Elateridae
Pleonomus canaliculatus (Faldermann)	Seed, seedlings	1
Melolonthidae
Apogonia cribricollis (Burmeister)	Larvae and adults; roots, leaves	1
Nitidulidae
Haptonchus luteolus (Erichson)	Branch	1
Rutelidae
Adoretus sinicus (Burmeister)	Larvae and adults; roots, leaves	1
Adoretus tenuimaculatus (Waterhouse)	Larvae and adults; roots, leaves; variety of deciduous trees	1
Anomala corpulenta (Motschulsky)	Larvae and adults; roots, leaves; wide variety of deciduous trees	1
Popillia mutans (Newman)	Larvae and adults; roots, leaves	1
Scarabaeidae
Oxycetonia jucunda (Faldermann)	Larvae and adults; roots, ovulate strobilus	1
Potosia brevitarsis (Lewis)	Larvae and adults; roots, ovulate strobilus	1
Hemiptera
Cicadidae
Cryptotympana atrata (Fabricius)	Branch	1
Coccidae
Ceroplastes ceriferus (Fabricius)	Twig	2
Ceroplastes japonicas (Guaind)	Leaves; variety of shrubs and trees	1
Ceroplastes rubens (Maskell)		2
Cerostegia japonicus (Green)		2
Parthenolecanium corni (Bouché)		1
Diaspididae
Aulacaspis thoracica (Robinson)		1
Chrysomphalus aonidum (Linnaeus)		1
Criconemoides morgensis (Hofmanmer and Menzel) Taylor		2
Lepidosaphes kuwacola (Kuwayama)		2
Parlatoreopsis pyri (Marlatt)	Trunk, twig, leaf	2
Parlatoria pergandii (Comstock)		1
Pseudaulacaspis cockerelli (Cooley)	Variety of shrubs and deciduous trees	1
Pseudaulacaspis pentagona (Targioni Tozzetti)		1
Pseudaulacaspis pentagona (Targioni-Tozzetti)		2
Unaspis yanonensis (Kuwana)		1
Flatidae
Geisha distsndissima (Walker)		1
Margarodidae
Drosicha corpulenta (Kuwana)		1
Icerya purchasi (Maskell)		1
Pentatomidae
Erthesina fullo (Thunberg)		1
Plautia fimbriata (Fabricius)		1
Pseudococcidae
Pseudococcus comstoki (Kuwana)	Leave, twig	2
Pseudococcus maritimus (Ehrhorn)		1
Ricaniidae
Euricania ocellus (Walk.)		1
Ricania speculum (Walker)		1
Scutelleridae
Solenostethium rubropunctatum (Guenrin)		1
Hymenoptera
Eurytomidae
Eurytoma samsonovi (Vassiliev)	Seed	1
Lepidoptera
Carposinidae
Carposina sasakii (Matsumura)	Seed	1
Cossidae
Arbela dea (Swinhoe)		1
Holcocerus insularis (Staudinger)		1
Holcocerus vicarius (Walker)	Larvae; trunk; variety of trees	1, 2
Zeuzera coffeae (Nietner)	A variety of trees	1
Zeuzera leuconotum (Butler)		1
Crambidae
Archernis tropicalis (Walker)	Bud, leaves	1
Dichocrocis punctiferalis (Guenée)	Larvae; seeds; wide variety of trees and crops	1
Erebidae
Euproctis digramma (Collenette)	Bud, leaves	1
Euproctis flava (Fabricius)	Bud, leaves	1
Euproctis pseudoconspersa (Strand)	Bud, leaves	1
Hyphantria cunea (Drury)	Flower buds, bark	2
Lymantria dispar (Linnaeus)	Bud, leaves	1
Miltochrista delineata (Walker)	Bud, leaves	1
Spilarctia subcarnea (Walker)	Leaf-mining herbivores	2
Spilosoma subcarmeum (Walker)	Flower buds, bark	2
Geometridae
Buzura suppressaria (Guenée)	Bud, leaves	1
Culcula panterinaria (Bremer & Grey)	Bud, leaves	1
Napocheima robiniae (Chu)		2
Ophthalmodes sp.	Bud, leaves	1
Hepialidae
Phassus excrescens (Butler)		2
Lasiocampidae
Cyclophragma undans (Walker)	Bud, leaves	1
Lebeda nobilis (Walker)	Bud, leaves	1
Malacosoma spp.	Bud, leaves	1
Paralebeda plagifera (Walker)	Bud, leaves	1
Limacodidae
Cania bilineata (Walker)	Bud, leaves	1
Chalcocelis albiguttatus (Snellen)	Bud, leaves	1
Cnidocampa flavescens (Walker)	Larvae; leaves; wide variety of deciduous trees	1, 2
Iragoides conjuncta (Walker)	Bud, leaves	1
Setora postornata (Hampson)	Bud, leaves	1, 2
Thosea sinensis (Walker)	Bud, leaves	1
Lymantriidae
Ocneria disper L. (Lymantridae)		2
Noctuidae
Adris tyrannus (Guenée)	Adults; seeds, branches; variety of fruit trees	1
Agrotis ipsilon (Hufnagel)	Seedlings	1
Agrotis tokionis (Butler)	Seedlings	1
Heliothis armigera (Hübner)	Larvae; leaves; wide variety of crops and Ginkgo	1
Prodenia litura (Fabricius)	Larvae; leaves; wide variety of deciduous trees and crops	1
Psychidae
Acanthopsyche sp.	Bud, leaves	1
Chalia larminati (Heylearts)	Bud, leaves	1
Chalioides kondonis (Matsumura)	Bud, leaves	1
Cryptothelea minuscula (Butler)	Bud, leaves	1
Cryptothelea variegata (Snellen)	Larvae; leaves; wide variety of deciduous trees, sometimes crops	1, 2
Eumeta japonica (Heylaerts)	Flower buds, bark	2
Eumeta minuscula (Butler)	Flower buds, bark	2
Pyralidae
Etiella zinckenella (Treitschke)	Seed	1
Saturniidae
Dictyoploca japonica (Moore)	Larvae; leaves, flower buds; wide variety of deciduous trees	1, 2
Eriogyna pyretorum (Westwood)	Larvae; leaves; wide variety of deciduous trees	1, 2
Tortricidae
Archips argyrospilus (Walker)	A contaminant of pollen-derived tissue culture	2
Archips compacta (Meyrick)	Bud, leaves	1
Archips crataegana (Hubner)	Bud, leaves	1
Archips eucroca (Diakonoff)	Bud, leaves	1
Archips fuscocupreanus (Walsingham)	Flower buds, bark	2
Cacoecimorpha pronubana (Hubner)		3
Choristoneura longicellana (Walsinghaam)	Bud, leaves	1
Grapholita funebrana (Treitschke)	Seed	1
Grapholitha molesta (Busck)	Seed	1
Homona coffearia (Nietner)	Bud, leaves	1
Homona magnaima (Diakonoff)	Bud, leaves	1
Homona magnanima (Diakonoff)	Leaf-mining herbivores	2
Pammene ginkgoicola (Liu)	Larvae; short shoot; ginkgo only	1
Spilonota ocellana (Schiffermuller et Denis)	Larvae; flower buds, leaves; a variety of fruit trees	1
Orthoptera
Acrididae
Chondracris rosea (De Geer)	Bud, leaves	1
Gryllidae
Brachytrupes portentosus (Lichtenstein)	Seed, seedlings	1
Gryllus testaceus (Walker)	Seed, seedlings	1
Gryllotalpidae
Gryllotalpa orientalis (Burmeister)		1
Gryllotalpa unispina (Saussure)		1
Tettigoniidae
Elimaea chloria (Haan) Det	Branch	1
Elimaea punctifera (Walker)	Branch	1
Holochlora nawae (S.Matsumura & Shiraki)	Branch	1
Prostigmata
Tarsonemidae
Polyphagotarsonemus latus (Banks)		1
Tetranychidae
Panonychus ulmi (Koch)		1
Tetranychus viennensis (Zacher)		1
Rhabditida
Heteroderidae
Heterodera marioni (Cornu) Marcinowsk	Root	3
Meloidogynidae
Meloidogyne sp.	Root	3
Thysanoptera
Thripidae
Scirtothrips dorsalis (Hood)	Larvae; buds, leaves; wide variety of shrubs and Ginkgo	1

• 1. Cao (2007); 2. Hori et al. (1997); 3. Begović Bego (2011).

Given their frequent occurrences, most relevant studies put emphasis on Dictyoploca japonica, P. ginkgoicola, S. dorsalis and several beetles (Coleoptera, Scarabaeidae). Detailed descriptions are as follows.

9.1.1 Dictyoploca japonica Moore

Dictyoploca japonica Moore (Lepidoptera, Saturniidae), the Japanese giant silkworm, which is also known as Ginkgo giant silkworm moth in China, is the predominant Ginkgo defoliator. Its fifth instar larvae can consume the entire leaf and even lead to a bare crown (Cao, 2007; Xu, 2018). It has been observed in Ginkgo plantations over 19 provinces in China and mainly occurred on trees older than 20 years (Cao, 2007). It produces one generation per year and overwinters as eggs (Cao, 2007). The growth rate of its eggs increased under warmer and wetter conditions (Huang, 1983; Sun et al., 1991). Its hibernating eggs start to develop at 4.5°C and hatch when the mean daily temperature reaches 15°C (Li, 2010a, 2010b). The larvae dispersed to the whole tree at the third instar, and the major leaf consumption occurred from the fourth to the sixth instar (Cao, 2007; Li, 2010a, 2010b).

Effective chemical pesticides against the larvae of Dictyoploca japonica are listed in Table S4. Biopesticides like Bacillus thuringiensis, Beauveria bassiana, abamectin, chlorbenzuron and triflumuron have been proven effective as well (Dong, 2013; Li et al., 2009; Wang et al., 2012; Yang et al., 2001). Moreover, applying nuclear polyhedrosis virus is also a biological control method for the Japanese giant silkworm (Sun et al., 1989). Other natural enemies of this moth include Trichogramma spp. (Hymenoptera, Trichogrammatidae) (Huang, 1983), Anastatus spp. (Hymenoptera, Eupelmidae), Apanteles spp. (Hymenoptera, Braconidae), Pica pica L. (Passeriformes, Corvidae) and Garrulax canorus L. (Passeriformes, Leiothrichidae) (Jiang et al., 2015; Wu et al., 2001). Artificial cocoon removal and egg burning are also effective controlling methods (He, 1998; Li et al., 2009).

9.1.2 Pammene ginkgoicola Liu

Pammene ginkgoicola Liu (Lepidoptera, Tortricidae) is a moth that mainly feeds on short shoots and branchlets. It causes damage exclusively to Ginkgo (Cao, 2007). It prevails in many cities across China (Zhang & Li, 1981). Seed production in plantations can be reduced by 10%–15% (more than 70% in the worst case) owing to this pest in Rugao county, Jiangsu province (Zou & Zuo, 1998). Young trees with thin, smooth barks were rarely harmed, since P. ginkgoicola can only pupate in bark thicker than 6 mm (Jiang et al., 1996; Zhang & Li, 1981). Also, well-grown Ginkgo with a dense crown was less infected by this moth (Jiang et al., 1996, 1998).

It produces one generation annually and overwinters as pupae. From late April to late June, the larvae begin to damage Ginkgo (Cao, 2007; Jiang et al., 1996; Jiang et al., 1998; Li, 1994; Zhang & Li, 1981). After 1–2 days from hatching, the larvae bore into the short shoot and consume leaves nearby (Cao, 2007). During pupation, the larvae pupate in the stem or old branches at a height of 1.5–6.0 m above-ground (Li, 1994). Pupation was more common on the sunny side of the tree trunk than that on the shade side (Jiang et al., 1996).

Effective chemical pesticides against P. ginkgoicola are listed in Table S4. Bacillus thuringiensis Berliner, Beauveria bassiana (Bals.) Vuil., Coccinellidae spp., Araneae spp. and Myrmeleontidae spp. were proven efficient biological pesticides (Li, 1994; Yang, 2015).

9.1.3 Scirtothrips dorsalis Hood

The adults and nymphs of S. dorsalis Hood (Thysanoptera, Thripidae), known as the tea yellow thrips, suck on Ginkgo leaves (Cao, 2007). Generally, the first generation occurs in mid-May. Then, it began to cause great damage to the leaves before its rapid population decline in September (Feng et al., 2013; Zhang & Wang, 1991). In July, the density of the tea yellow thrips can reach to 300 per leaf (Zhang & Wang, 1991). Ginkgo leaves infested by the tea yellow thrips showed a lower growth rate of leaf area and weight as well as lower contents of chlorophyll, soluble sugar and soluble protein (Qu, 2009).

Chemical pesticides against the larvae of S. dorsalis are listed in Table S4. Several spiders, including Erigonidium graminicola Sundevall (Araneae, Linyphiidae), Theridion octomaculatum Bösenberg & Strand (Araneae, Theridiidae), Clubiona reichlini (Araneae, Clubionidae) and Hylyphantes graminicola (Araneae, Linyphiidae) are the main predators of S. dorsalis (Ke et al., 2010; Li, 2010a, 2010b).

9.2 Plant parasites

Ginkgo can host various fungi (Table 4) and bacteria on different plant parts. The bacterial communities mainly comprise members of Acidobacteria, Actinobacteria, Bacteroidetes and Proteobacteria (Leff et al., 2015). Four Ginkgo leaf diseases caused by fungi have been observed including black rot, anthracnose, leaf spot and target spot, caused by four pathogens, Alternaria alternata (Fr.) Keissl. (Pleosporales, Pleosporaceae), Colletotrichum sp. (Glomerellales, Glomerellaceae), Phyllosticta ginkgo Brunand (Botryosphaeriales, Phyllostictaceae) and Pestalotiopsis ginkgo Hori (Amphisphaeriales, Pestalotiopsidaceae) respectively (Chen, 2010).

TABLE 4. Fungi (by Order) directly associated with Ginkgo biloba world-wide, not including those found on soil or litter below the trees, or those found solely on dead wood. Nomenclature follows that of the Database of Global Biodiversity Information Facility or Database of European or Mediterranean Plant Protection Organization

Species/classification	Ecological notes
Ascomycota
Amphisphaeriales
Pestalotia ginkgo Hori	Pestalotia disease
Pestalotiopsis ginkgo Hori	Leaf spots
Botryosphaeriales
Macrophomina phaseoli (Maubl.) S.F.Ashby
Phyllosticta ginkgo Brunaud	Leaf spots
Dothideales
Gonatobotryum apiculatum (Peck) S.Hughes
Eurotiales
Aspergillus spp.	Seeds
Eurotium chevalieri L. Mangin
Penicillium spp.	Seeds
Spicaria sp.	Seeds
Glomerellales
Colletotrichum gloeosporioides (Penz.) Penz. & Sacc.	Leaf spots
Colletotrichum sp.	Leaf spots
Glomerella cingulata (Stoneman) Spauld. & H.Schrenk	Anthracnose; leaf spots
Helotiales
Botryotinia fuckeliana (de Bary) Whetzel	Grey mould
Hypocreales
Fusarium oxysporum Schltdl.	Root rot
Fusarium spp. (canker)
Trichoderma koningii Oudem.	Seeds
Pezizales
Phymatotrichum omnivorum Duggar	Root rot
Pleosporales
Alternaria alternata (Fr.) Keissl.
Alternaria sp.	Seeds
Hendersonia ginkgonis Naito	Brown leaf spot disease
Saccharomycetales
Geotrichum candidum Link.	Seeds
Sordariales
Chaetomium spp.
Xylariales
Rosellinia necatrix Berl. ex Prill.	White root rot
Xylaria nigrescens (Sacc.) Lloyd	Seed rot
Basidiomycota
Bartheletiales
Bartheletia paradoxa G.Arnaud
Cantharellales
Ceratobasidium anceps (Bres., Syd. & P.Syd.) H.S.Jacks.	Thread blight
Thanatephorus cucumeris (A.B.Frank) Donk	Web blight
Corticiales
Erythricium salmonicolor (Berk. & Broome) Burds.	Pink disease
Helicobasidiales
Helicobasidium mompa Nobuj.Tanaka	Violet root rot
Hymenochaetales
Oxyporus populinus (Schumach.) Donk	Sapwood or wound rot; sometimes found on living trees following injuries
Polyporales
Fomes conatus (Weinm.) Gill	Sapwood or wound rot; sometimes found on living trees following injuries
Polyporus spp.	Sapwood or wound rot; sometimes found on living trees following injuries
Zygomycota
Mucorales
Mucor racemosus Fresen.	Seeds

Penicillium spp. (Eurotiales, Trichocomaceae), Aspergillus spp. (Eurotiales, Trichocomacea) and Spicaria sp. (Eurotiales, Trichocomaceae) are predominant pathogens in Ginkgo seed storage, followed by Geotrichum candidum Link. (Saccharomycetales, Dipodascaceae), Alternaria sp. (Pleosporales, Pleosporaceae), Trichoderma koningii Oudem. (Hypocreales, Hypocreaceae) and Mucor racemosus Fresen. (Mucorales, Mucoraceae), which can proliferate on the surface of seeds (Huang et al., 1998).

Alternaria alternata, Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. (Glomerellales, Glomerellaceae) and Pestalotia ginkgo Hori (Amphisphaeriales, Amphisphaeriaceae), which were reported to cause serious diseases on Ginkgo leaves, can overwinter in winter bud tissues, whereas only A. alternata can continue to infect young leaves in the next spring (Zhu, 1993). Alternaria alternata can exist in large amounts on the fallen leaves. After winter, they continuously form conidia on sporophores which consequently infect healthy leaves (Zhu, 1993). Pestalotiopsis ginkgo infects the leaves through stomata or penetrate the epidermis directly on the adaxial surface of leaves (Chen, 2010).

Fusarium oxysporum Schltdl. (Hypocreales, Nectriaceae) was reported to be the main pathogen responsible for root rot (Diao et al., 2015). An antibacterial protein, ginkbilobin, has an inhibitory effect on five fungi including Fusarium oxysporum (Wang & Ng, 2000). The biological agent produced from Bacillus subtilis (Ehrenberg) Cohn (Bacillales, Bacillaceae) also controls the growth of Fusarium oxysporum (Diao et al., 2015). Hori et al. (1997) listed 36 saprophytes in leaf litters collected from Japan. Another interesting saprophyte, Bartheletia paradoxa G. Arnaud (Bartheletiales, Bartheletiaceae), shows strong host selectivity but causes no diseases.

9.3 Plant diseases

Diseases caused by pathogens are mainly stem rot and leaf blight. Stem rot mainly affects young trees, especially in 1–3 years after transplantation (Shi, 1999). Mortality rate of young Ginkgo due to this disease was up to 31.8%, but generally 5%–12% in China (Shi, 1999). The pathogen responsible for seedling stem rot is Macrophomina phaseoli (Maubl.) S. F. Ashby (Botryosphaeriales, Botryosphaeriaceae) (Cao, 2007). Long exposure to high temperature or drought stress could reduce the resistance of Ginkgo to this pathogen (Shi, 1999). A solution of 50% Tuzet, 50% carbendazine and 70% thiophanate-methyl has been proven efficient in the treatment of stem rot (Sun et al., 2001). Shading (4 consecutive hours) and application of organic fertiliser can effectively reduce the occurrence of stem rot on seedlings (Fang et al., 1956).

In the early 1960s, leaf blight was reported from one of the Ginkgo nurseries in Taizhou city, Jiangsu province (Cao, 2007). It was caused by the infection of three pathogenic fungi, namely A. alternata, C. gloeosporioides and Pestalotia ginkgo (Cao, 2007; Zhou, Liao, & Huang, 2001; Zhu & Shi, 1991). From 1987 to 1988, the incidence of leaf blight reached 100% in Jiangsu province (Shi & Zhu, 1989). In 2014, Ginkgo blight was still common in northern Nanjing city, Jiangsu province, with an average incidence rate of 100% in early June (Zhang, You, et al., 2019). Symptoms of leaf blight include four types, namely the yellow edge, the disease spot, withered and uniformly turning yellow (Zhang, You, et al., 2019). After 7 days from the infection of A. alternata, the disease spot accounted for half of the leaf area (Zhou et al., 2000). Leaf blight can reduce the contents of chlorophyll a and chlorophyll b, and increase the water loss from non-stomatal pathways in leaves (Lu et al., 2016). Bilobetin, ginkgetin and 7-O-methylamentoflavone extracted from T. baccata and Ginkgo could significantly inhibit the growth of A. alternata (Krauze-Baranowska & Wiwart, 2003). The antimicrobial peptides isolated from Ginkgo, known as GAFP, conferred resistance to A. alternata (Huang et al., 2000). However, leaf blight can reduce the content of flavonoids in Ginkgo leaves leading to weaker resistance to pathogens (Lu et al., 2016).

Warm temperature (above 20°C) and high relative humidity (above 90%) could promote the initial occurrence of leaf blight (He et al., 2004), whereas low spring temperature would postpone initial infection (Zhou et al., 2001). Female Ginkgo trees showed weaker resistance to leaf blight than the male ones since they tend to allocate more energy to reproductive organs (Shi & Zhu, 1989). The susceptibility to leaf blight was also related to fertilisation management and cultivation approaches (Shi & Zhu, 1989). Experiments showed that 45% carbendazim, 50% Tuzet and alternative sprayings of propiconazo, iprodione and thiophanate-methyl can be applied for the prevention of leaf blight, while tebuconazole can treat leaf blight at its incipient stage (He et al., 2004; Zhou et al., 2003). Other fungicides include 40% carbendazim, 90% fosetyl-aluminium, 20% triadimefon and amicarthiazol (Shi & Zhu, 1989; Zhu et al., 1994). The application of iprodione, thiophanate-methyl and carbendazim was proven effective to inhibit the growth of A. alternata and Pestalotia ginkgo (Zhou, Huang, et al., 2001).

10 HISTORY

10.1 Evolutionary history

Ginkgo plants, or Ginkgophytes, usually refer to Ginkgoales which are composed of Ginkgo and its fossil relatives (Zhou et al., 2020). Phylogenetic analysis based on plastome data showed that the stem group age of Ginkgoaceae was approximately 325 mya (Hohmann et al., 2018). The oldest fossil record of Ginkgoales dates back to the early Permian (c. 270 mya), or even to the Carboniferous (c. 320 mya) (Florin, 1936; Høeg, 1967; Naugolnykh, 1995).

With their strong tolerance to harsh environmental conditions, Ginkgophytes survived the Permian–Triassic extinction event and entered a stage of rapid radiation in the late Triassic (Zhou et al., 2020). The diversity pattern of Ginkgoales formed in the late Triassic initially and further developed in the Jurassic and the early Cretaceous (Zhou, 2009). The only extant group of Ginkgophytes, Ginkgo L., appeared about 180 mya in the Jurassic (Tralau, 1967, 1968). Ginkgo yimaensis, unearthed in Henan province, central China, was reported the most complete and oldest fossil species in Ginkgo (Jurassic). The extant G. biloba diverged from its sister Ginkgo adiantoides around 56 mya (Crane et al., 1990; Zhou et al., 2012).

The evolutionary history of Ginkgophytes left discernible imprints in fossils (Zhou, 2003). The evolution of vegetative organs in Ginkgoales was marked by the appearance of short branches and petioles (Zhou et al., 2020). The Palaeozoic Ginkgophytes like Trichopitys Saporta and Sphenobaiera Florin had only long branches and the short branches did not appear until the late Triassic (Anderson & Anderson, 2003). Available fossil records of Ginkgoales clearly showed an evolutionary trend towards simplification since the late Triassic (Zhou, 2003). The leaf became flat, webbed, less lobed and enlarged along its evolution (Zhou, 2003). Seed size increased while the individual ovule stalk (pedicel) shortened and finally disappeared. Represented by G. yimaensis, the Jurassic Ginkgo ovulate organs had three or four mature ovules, each terminating in a long individual stalk. The Cretaceous ovulated organs represented by G. apodes were more similar to modern Ginkgo, with no individual stalk and several ovules (Zhou & Zheng, 2003). Ginkgo adiantoides from the Palaeocene, which was sister to Ginkgo, showed the modern ovule type (Crane et al., 1990; Zhou & Zheng, 2003). Pollen-bearing fossils of Ginkgoales were scarce earlier than the late Triassic (Harris et al., 1974; Heer, 1876; Konijnenburg-van Cittert, 2010; Naugolnykh, 2018; Zhang, Lenz, et al., 2020), but the abundant fossil records later exhibited an evolutionary tendency to simplification (Liu et al., 2006; Rothwell & Holt, 1997; Zhou et al., 2020).

Ginkgoales began to decline and to go extinct since the late Cretaceous (Crane et al., 1990; Hill & Carpenter, 1999; Isah, 2015; Stewart & Rothwell, 1993; Zhou et al., 2020). Ginkgo may have gone extinct in North America by the late Miocene (c. 10 mya), then in Europe by the Pliocene c. 1.7 mya) (Kovar-Eder et al., 1994; Tralau, 1967, 1968; Wolfe, 1987; Zhou, 2003). The great upheavals of the earth and the following ice age during the Tertiary and the Quaternary destroyed Ginkgo in most parts of the world (Major, 1967; Uemura, 1997). The extinction was mildest in east Asia, where complex habitat mosaics of mountain topography facilitated orographic precipitation (Tang et al., 2018).

There are two well-recognised glacial refugia of Ginkgo in south-western and eastern China represented by Mt. Dalou (including Mt. Jinfo) (Tang et al., 2012) and Mt. Tianmu, Zhejiang province respectively (Gong et al., 2008). Although the ancient Ginkgo population in Mt. Tianmu was previously thought to be introduced by monks (Wu et al., 1992), increasing lines of evidence from molecular studies indicate that wild Ginkgo population exists in Mt. Tianmu (Gong et al., 2008; Ling & Zhang, 2004; Xie, 2014; Zhao et al., 2016, 2019). Besides Ginkgo refugia in eastern and south-western China, a third refugium located in southern China (represented by Xing’an, Guangxi province and Nanxiong, Guangdong province; Figure 1) was identified based on genome resequencing data (545 trees world-wide) and population genomics. Simulation of demographic history suggested that the lineage divergence of all living Ginkgo was initiated 515,000 years ago, when the south-western populations in China were separated from others, followed by the divergence between eastern and southern refugia populations 318,000 years ago. As a result of admixture between the south-western and southern refugia populations, the central and northern China populations originated 139,000 years ago. These evolutionary events may have been driven by climatic oscillation during the Pleistocene glaciation.

10.2 Introduction history

Historical records and molecular evidence suggest that human migration and managements have strongly promoted the dispersal of Ginkgo which shaped its current global distribution (Gong et al., 2008; Zhao et al., 2010, 2019). Ginkgo has a long history of cultivation in China where Ginkgo trees over 1000 years old are not rare. During the Three Kingdoms Period (220–280), Ginkgo was widely cultivated in the Yangtze valley, then being massively planted northwards (He et al., 1997).

The first overseas introduction of Ginkgo trees dates back to the sixth century (the Tang Dynasty) when people might have carried it from China to the Korean Peninsula via land transplantation and then shipped it to Japan (Zhao et al., 2010). Beginning in the seventh century, cultural and commercial connections between China and Japan largely facilitated the introduction of Ginkgo into Japan (Cao, 2007). The initial arrival may have occurred in western Japan followed by further dissemination to eastern Japan via propagation using seeds and cuttings (Katakura et al., 2019). The oldest female Ginkgo tree in Toyama, Japan, is probably more than 1500 years old, which fits well with the history of cultural and agricultural human activities in the vicinity of the Ginkgo population (Zhao et al., 2010).

Engelbert Kaempfer, a German physician and botanist, visited Japan from 1690 to 1692, where he saw the Ginkgo and described it in his work Amoenitatum exoticarum (Kaempfer, 1712). By 1730 after his death, the first Ginkgo tree was planted in Utrecht, the Netherlands (Cao, 2007; Li et al., 1981). Ginkgo was increasingly planted all over Europe later: Geetbets (Belgium) 1730 (independently brought by missionaries from China), Anduze (France) 1750, Padova (Italy) 1750, Slavkov (Czech Republic) 1758, Kew (United Kingdom) 1762, Vienna (Austria) 1770, Daruvar (Croatia) 1777, Harbke (Germany) 1781 and Montpellier (France) 1788. The first recorded female Ginkgo tree in Europe was planted near Geneva, Switzerland, and its scions were grafted onto a male tree and produced seeds (The Ginkgo Pages, 2021; Zhao et al., 2010). Similar grafted female scions with fertility were also produced at the Vienna Botanical Garden.

The first Ginkgo tree in America, which is male, was planted in Hamilton private estate, Philadelphia in 1784 (Del Tredici, 1981). The first fertile female Ginkgo in the United States was planted in Frankfurt, over 160 years ago (Del Tredici, 1981; Xing et al., 1994). In the early 19th century, Ginkgo was introduced to many states of the United States, especially in private estates. Then, Ginkgo was planted along the East Coast massively from the late 19th to the early 20th century (Xing, 2013).

Evidence from population genomics suggested no refugial populations outside China and that all overseas populations in Japan, Korea, Europe and America were introduced from eastern China, indicating the importance of the Ginkgo population inhabiting Mt. Tianmu in its global redistribution mediated by humans (Zhao et al., 2019). There is evidence that the oldest Ginkgo trees in Europe were introduced from eastern China rather than from Japan. This might have resulted from the introduction via trade between eastern Asia and Europe in the 18th century. It can also be inferred that old Ginkgo trees in the United States were sourced from Europe historically, as well as from China in recent decades.

10.3 Taxonomic history

The taxonomic state of Ginkgo had experienced long-standing disputes (syn. Salisburia adiantifolia Sm., Salisburia biloba (L.) Hoffmanns., Ginkgo macrophylla K. Koch, Salisburia ginkgo Rich., Salisburia macrophylla Reyn., Pterophyllus salisburiensis J. Nelson, G. biloba f. aurea (J. Nelson) Beissn., G.biloba f. fastigiata (A. Henry) Rehder, G. biloba f. laciniata (Carrière) Beissn., G. biloba f. microsperma Sugim., G. biloba f. parvifolia Sugim., G. biloba f. pendula (Van Geert) Beissn., G. biloba f. variegata (Carrière) Beissn., G. biloba var. aurea (J. Nelson) A. Henry, G. biloba var. epiphylla Makino, G. biloba var. fastigiata A. Henry, G. biloba var. laciniata (Carrière) Carrière, G. biloba var. pendula (Van Geert) Carrière, G. biloba var. variegata (Carrière) Carrière, S. adiantifolia var. laciniata (Carrière). Carl Linnaeus (1771) described Ginkgo scientifically shortly after its introduction to Europe. However, there was no consensus on which taxonomic group it should belong to during the 18th and 19th centuries. Hirase (1896) observed the release of swimming sperm from pollen tubes during fertilisation, which was totally different from pines. This unique feature triggered botanists to conduct comprehensive studies of the morphology, anatomical structure and biological properties of Ginkgo in the following decades (Chamberlain, 1935; Seward, 1900, 1919; Shimamura, 1937).

Since then, various approaches have been applied to determine the evolutionary affinity between Ginkgo and other gymnosperms. Based on 95 traits, phylogenetic analysis failed to resolve the relationship between several gymnosperms including Ginkgo (Rothwell & Serbet, 1994). Based on evidence from morphology and anatomy, Ginkgo was suggested to be similar to Cordaitopsida and Coniferopsida in the woods and leaves (Crane, 1985; Doyle & Donoghue, 1986, 1987a, 1987b). However, Ginkgo was considered more similar to cycads in pollen morphology, reproductive behaviour and embryology (Hori & Miyamura, 1997; Wang & Chen, 1983). Based on DNA sequences, recent phylogenetic analyses supported that Ginkgo was sister to Cycadidae (Hohmann et al., 2018; Lee et al., 2011; Ran et al., 2018; Ruhfel et al., 2014; Wu, Chaw, et al., 2013; Xi et al., 2013).

10.4 Uses

Ginkgo is of great value in medicine, food, horticulture, art and religion (Cheng & Fu, 1978; Hori & Hori, 1997). The medical value of Ginkgo has long been recognised. The Ginkgo seed was used as a crude drug to treat cough, bronchial asthma, irritable bladder and alcohol abuse in China and Japan for more than 700 years (Chinese Pharmacopoeia Commission, 2020; Guo et al., 2018; Hori & Hori, 1997; Leistner & Drewke, 2010; Wada & Haga, 1997). In European medicine, Ginkgo leaves were used to treat insufficient blood flow, cerebral insufficiency, memory deficits, disturbances in concentration, depression, dizziness, tinnitus, vertigo, headache, learning disability and intermittent claudication (Juretzek, 1997; van Beek, 2000). Ginkgo extract, which showed remarkable protective effects against various toxins and radiations (Omidkhoda et al., 2019), has been one of the best-selling herbal remedies in America and many European countries (Kressman et al., 2010). Terpenoids and flavonoids are two main pharmacological components in Ginkgo extracts (Jacobs & Browner, 2000; Juretzek, 1997). EGb761, the only well-studied Ginkgo extract at present, has shown beneficial effects on the treatment of vascular disease and neurodegenerative disease such as Alzheimer-type dementia and insufficient blood flow (Arenz et al., 1996; Juretzek, 1997; Luo et al., 2002; Schmid, 1997; Tu et al., 2020; Weinmann et al., 2010; Zhang, Liu, et al., 2020).

For thousands of years, the endosperm of Ginkgo seed has been considered edible in some parts of the world, especially in China and Japan, where people believed that it was beneficial to health (Cheng & Fu, 1978; Major, 1967). According to literature, Ginkgo has been used as a source of nuts since at least 2000 years ago in the Han Dynasty in China (Liang, 1993). However, excessive consumption of Ginkgo seeds could cause intoxications characterised by tonic–clonic convulsions and vomiting (Cao, 1999a; Kobayashi, 2019; Yagi et al., 1993). Ginkgotoxin, 4′-O-methylpyridoxine (MPN), along with its glycosides have been proven to be the causal compounds of those symptoms (Wada et al., 1985; Wada et al., 1988; Scott et al., 2000; Yoshimura et al., 2006; Leistner & Drewke, 2010; Kobayashi et al., 2011; Kobayashi, 2019).

Ginkgo is also a valuable timber tree with light yellow sapwood and yellow-brown heartwood (Cheng & Fu, 1978). With light and soft texture, rich elasticity and delicate structure, Ginkgo wood is widely used in furniture, interior decoration, engraving, drawing boards and artwares like chessmen and oriental lacquerware (Cheng & Fu, 1978; Major, 1967).

The beautiful yellow leaves in autumn, a source of shade along streets and strong resistance to disease make Ginkgo a popular street and park tree (Cheng & Fu, 1978; Major, 1967). Several cultivars of Ginkgo have been nurtured for ornamental purposes with seed-bearing leaves, constant yellow leaves or different leaf shapes (Isah, 2015; Santamour et al., 1983; Xing et al., 1994).

Ginkgo has important value in culture and art. It is common in poetry, sculpture, painting and other artworks. Ancient Chinese people painted Ginkgo leaves on stone bricks in the Han Dynasty for aesthetic reasons (You, 1980). Exquisite Ginkgo xylotheques combining samples of woods with botanical illustrations from the Early Meiji period are housed in the Berlin-Dahlem Botanical Garden and Botanical Museum and the Royal Botanic Gardens, Kew (Nagata et al., 2013). The name ‘Ginkgo’ is probably derived from the transliteration of its Japanese dialect name ‘Yin-kyo’ or the Chinese name ‘Yin-hsing’, which both mean silver fruit (Isah, 2015; Nagata et al., 2015). The ancient Chinese named Ginkgo ‘duck foot tree’ given its leaf shape. Ginkgo is also known as Maidenhair tree given the resemblance of its fan-shaped leaves to those of Maidenhair ferns (Adiantum spp.) (The Editors of Encyclopaedia Britannica, 2021). Moreover, Ginkgo is the city tree of many cities in China including Linyi (Shandong province), Chengdu (Sichuan province), Dandong (Liaoning province) and Huzhou (Zhejiang province). Ginkgo also has important religious meaning and was planted as an alternative to the bodhi tree (Ficus religiosa) (Cao, 2007). In parts of Japan, Ginkgo was widely planted given its status in Confucian beliefs (Isah, 2015).

11 CONSERVATION AND MANAGEMENT

Ginkgo biloba is an endangered plant on the IUCN red list of threatened species (Sun, 1998). It is also on the List of Wild Plants under State Priority Conservation (first-class state) in China, the Red Book of Chinese Plants and China Species Red List (Fu & Jin, 1992; National Forestry and Grassland Administration of China, 2021; Wang & Xie, 2004). It has long been a debate whether Ginkgo deserves a priority conservation. Some people hold the view that no wild population exists anymore, or that Ginkgo has entered an extinction vortex which makes conservation efforts inefficient. However, population genomics and field survey identified natural populations in four regions of China (Zhao et al., 2019) (Figure 1). The hypothesis of extinction vortex was also refuted by lines of evidence including resilience of both population size and range to climatic oscillation and adaptive evolution of defence/response genes (Zhao et al., 2019). Moreover, the few natural populations identified in south-western China are distributed separately, with small population sizes of less than 100 individuals. Our field survey in Mt. Tianmu recorded 492 Ginkgo trees in total, which is still an extremely low number. A striking phenomenon is that few seedlings or juvenile trees were observed in most wild populations (Del Tredici et al., 1992; Xie, 2014). Thus, wild populations of Ginkgo call for conservation priority. During the past two decades, our group and the reserve administration carried out long-term field surveys of Ginkgo forests in Mt. Tianmu National Nature Reserve. To facilitate in situ conservation, a total of 290 Ginkgo trees were located, tag-numbered, inventoried and monitored; and 27 long-term Ginkgo plots of 20 m × 20 m were established (Gu et al., 2021; Lin et al., 2022). We launched a number of monitoring projects on the Ginkgo microhabitats, DBH growth rate, seedling survival and seed predators in Mt. Tianmu (Gu et al., 2021; Lin et al., 2022). Field and manipulative experiments were carried out to test a number of factors or processes speculated to be associated with the regeneration restriction. We also implemented ex situ conservation since 2017 by seed preservation in Zhejiang University and seed germination and seedling conservation in Zhejiang Forestry Academy. Meanwhile, local and religious beliefs may have played an important role in conserving Ginkgo forests in China. Indigenous people and immigrants in Mt. Dalou have strict traditional taboos against planting or cutting down Ginkgo, leading to the effective preservation of wild Ginkgo trees there (Huang et al., 2020; Tang et al., 2012; Xiang & Xiang, 1997). The oldest cultivated Ginkgo trees can be found near Taoist and Buddhist temples, where the survival of these trees has benefited from monks (Isah, 2015).

It has been argued that the growing supply of cultivated Ginkgo cannot meet the soaring commercial demand in medical and other fields, thus threatening the survival of natural populations (Masood, 1997). The development of large-scale artificial propagation of Ginkgo might dispel such concerns to some extent (Schmid, 1997). However, logging is still a major threat to many natural Ginkgo populations (Sun, 1998). Other threats include the lack of sunny microsites suitable for seedling growth, seed collection by people or seed predation by animals (Del Tredici et al., 1992).

Practice has shown that Ginkgo has a very wide range of adaptability. According to different climate forecasts, the suitable habitat of Ginkgo would move towards higher latitude and altitude (Guo, Guo, et al., 2019; Guo, Lu, et al., 2019). Considering the poor natural dispersal ability of Ginkgo, changing climate may nevertheless have a negative impact on its conservation.

12 GLOBAL HETEROGENEITY

Ginkgo is native to China. All Ginkgo trees present outside China are introduced. This clearly limits its global ecological heterogeneity. Here, we focus on how microcosmic behaviour of Ginkgo varies in different parts of the world. Concentrations of some heavy metal and mineral nutrient elements in Ginkgo leaves differ significantly between China and Europe. For example, in Jiangsu province, China, the average K concentration, average Ca concentration, average Mg concentration and average Fe concentration are 9320, 25,240, 4360 and 207 mg/kg (Wei et al., 1999), while those in Turkey are 2224, 11,970, 2467 and 373 mg/kg (Ozyigit et al., 2018) respectively. Duarte et al. (2013) compared the leaf and stem microscopic characters of different Ginkgo specimens from South America (Curitiba, Brazil) and Asia (Beijing, China and Hiroshima and Tokyo, Japan). Their findings suggested that all Ginkgo specimens studied showed similar characters independently of their geographic origin or environments, except for the contents of phenolic compounds.

ACKNOWLEDGEMENTS

This study was supported by the National Key Research and Development Program of China (no. 2017YFA0605104) and the National Natural Science Foundation of China (no. 31870190, 32071484). The authors thank the editor and reviewers for their constructive comments that substantially improved the manuscript. They thank Ms. Jie-Ru Yan and Mr. Xin Zhang who helped improve English writing.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

AUTHORS' CONTRIBUTIONS

Y.-P.Z. conceived the ideas and supervised the work; H.-Y.L. designed the methodology; H.-Y.L., W.-H.L., C.-F.L. and H.-R.W. collected and analysed data; H.-Y.L. led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Open Research

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1111/1365-2745.13856.

DATA AVAILABILITY STATEMENT

Data are available from the figshare repository: https://doi.org/10.6084/m9.figshare.19126583.v1 (Lin et al., 2022). The same data are also available on the GinkgoDB website: https://ginkgo.zju.edu.cn/project/survey_data/2022.xlsx(Gu et al., 2021).