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An evolutionary and cultural biography of ginkgo
Abstract
Societal Impact statement
Ginkgo biloba is a distinctive living tree with a unique place in plant evolution and human culture. It is valued in horticulture and as a street tree, is a source of edible “nuts” and popular in herbal medicine, and it has proved inspirational in art, literature, and religion. Ginkgo is also a living link to diverse seed plants that flourished over 100 million years ago. With recent discoveries of extinct fossil ginkgo relatives, and the recent draft sequence of its genome, ginkgo offers opportunities to increase public understanding of plant science and the importance of plant conservation.
Summary
Ginkgo (Ginkgo biloba L.) is one of the world’s most distinctive trees and has no close living relatives. It is the last survivor of an ancient and once diverse lineage that was almost extinguished by the Pleistocene glaciations and survived only as a relic in restricted areas of eastern and central China. Remarkably, since then, through its association with people, ginkgo has undergone a dramatic resurgence. In China, Japan, and Korea, it has long been prized as an edible nut and it is also revered in eastern religions. Ginkgo is also one of the world’s most widely used street trees, has become a popular horticultural novelty, and has featured prominently in art of all kinds. Extracts from its leaves are a widely used herbal supplement. In the context of current threats to plant diversity, ginkgo is a good news story: an unusual exemplar that highlights how people can contribute to species survival in the world of plants.
Video Byte
An evolutionary and cultural biography of ginkgo
by Crane1 INTRODUCTION
With its distinctive branching and fan-shaped leaf, ginkgo is a tree that once seen is never forgotten (Figure 1a, b). Even those with the most slender interest in plants may know ginkgo as the tree with the smelly “fruits” or the source of a leaf extract that is good for your memory. But the unmistakable leaf, the acrid aroma of the fallen seeds, or the pills in the health food store, are only part of what makes ginkgo unique. Ginkgo is a botanical oddity, with no close living relatives. Its ancestors grew up with the dinosaurs and the single living species has come down to us almost unchanged for tens of millions of years. Ginkgo has one of the longest of all botanical pedigrees and Ginkgo biloba L., is a key species for studies of plant evolution (Crane, 2013; Hori et al., 1997).
Today, ginkgo is grown all over the world. It is a valuable street tree in urban landscapes. It has found a place in eastern spirituality, has inspired art of all kinds, and is also used in medicine, horticulture and eastern cuisines (Crane, 2013; Hori et al., 1997). In this article, I explore the evolutionary significance of ginkgo and trace its paleontological and cultural history; from its origin, proliferation, drastic decline and near extinction, to its ultimate renewal and resurgence at the hands of people.
2 REPRODUCTIVE BIOLOGY
Cycads, conifers, Gnetales, and angiosperms comprise the four main groups of living seed plants. Ginkgo is the fifth. But while there are almost half a million species of angiosperms and several hundred species of cycads, conifers, and Gnetales, G. biloba is the only living species of its lineage. It therefore occupies an important position in plant evolution and is a key point of reference for understanding a great variety of extinct plants. As the last survivor of a group that was once much more diverse, G. biloba may provide our best window into the biology and genetics of the diverse extinct seed plants that flourished between about 200 and 100 million years ago (Crane, 2013).
Once regarded as a cousin of pines, yews, and cypresses, ginkgo was first distinguished from conifers in plant classifications of the early 19th century. Ginkgo's distinctiveness was later confirmed by the discovery that the final phase of ginkgo reproduction, which results in the formation of the embryo, is very different from what occurs in conifers and all other trees. Ginkgo is dioecious. In the early spring, male trees produce pollen cones, and female trees produce ovule-bearing shoots with two young sessile ovules at the tip (Figure 1a). Each male tree produces vast numbers of pollen grains, which are released in perfect synchrony with the production of pollination drops from the developing ovules on female trees. Pollen trapped in the pollination drops sinks, is drawn into the ovule, and initiates the development of the food reserve for the future embryo. However, fertilization itself does not occur until several months later and the embryo, contained within the fleshy seed, is not mature until a few months later still (Figure 2a).
The final intimate details of ginkgo reproduction were first revealed in 1896 by the careful observations of Sakugoro Hirase, a botanical artist and technician working at the University of Tokyo (Hirase, 1896; Nagata, 1997). Hirase showed that each ginkgo pollen grain produces two sperm cells that swim to the egg propelled by a spiral band of rapidly beating flagellae. Soon after Hirase's discovery, the same phenomenon was also found to occur in cycads (Ikeno & Hirase, 1897), but this aspect of ginkgo and cycad reproductive biology is very different from the process of fertilization in conifers and all other trees. Just as egg-laying in the platypus recalls the reproductive biology of reptiles, the swimming sperm cells of ginkgo and cycads recall the reproductive biology of ferns. The recognition of swimming sperm in ginkgo was one of the most important early scientific discoveries made in Japan after the country emerged from its self-imposed isolation (Nagata, 1997) and it is of great significance for our understanding plant evolution.
3 EVOLUTION AND BIOGEOGRAPHY
Although G. biloba is the only living member of the ginkgo lineage, many kinds of extinct ginkgo-like plants existed in the past and have been recognized in the fossil record, in both the northern and southern hemispheres. Leaves not too different from those of modern ginkgo are especially well represented. Their distinctive fan-shaped form makes them easy to recognize, their thick cuticles and resinous leaf tissues make them resistant to decay, and there is also evidence that ginkgo often grew in habitats that are disproportionately well-represented in fossil assemblages. As a result, fossil ginkgo leaves are common in the paleobotanical record and often well-preserved (Crane, 2013).
Careful paleobotanical work by Zhou Zhiyan of the Nanjing Institute of Geology and Palaeontology has shown that several different kinds of ginkgo-like plants grew in China during the Jurassic period (200–145 Mya; Zhou & Zhang, 1989, 1992 ; Zhou, 2009; see Figure 1c). Fossil Ginkgo yimaensis, differed in only minor ways from living G. biloba. Its leaves were deeply divided, more like the sucker shoots and seedling leaves of living ginkgo rather than the mature foliage (Figure 1a, b), and the seeds were borne on individual stalks (Figure 1c) rather than sessile as in living G. biloba (Figure 1a). However, the fossil genera Yimaia and Karkenia were more distinct. Yimaia had leaves that were very deeply divided into narrow digitate lobes, and seeds that were borne in clusters. In Karkenia, the seeds were massed together in cone-like aggregations and each was borne on a distinct reflexed stalk (Figure 1c).
Despite their differences from G. biloba, fossils like G. yimaensis, Yimaia and Karkenia had unmistakably ginkgo-like fan-shaped leaves. However, increasing paleobotanical evidence shows that the ginkgo lineage also included plants with simple, strap-shaped, leaves, and reproductive structures very different from those of the living species. The ginkgo lineage seems to also have included plants like Umaltolepis (Herrera et al., 2017) and Umkomasia (Shi et al., 2016, 2018 ), which suggests links between ginkgo and other groups of extinct ancient plants (Shi et al., 2016, 2018 ). Exploring the morphological limits of the ginkgo lineage, and the relationship of ginkgo to other living and fossil seed plants, is currently an area of active research.
Ginkgo-like plants are first recognized in the Middle and Late Triassic period (248–206 Mya) and were especially diverse through the Late Triassic, Jurassic (206–144 Mya), and Early Cretaceous (144–99 Mya). Changes in the diversity of the ginkgo lineage over time are difficult to estimate, but evidence from both leaves and seed-bearing structures suggests that there was a pronounced decline in the mid-Cretaceous period, about 100 Mya, most likely in association with the rise of flowering plants (Crane, 2013; Zhiyan & Wu, 2006). By the time of the Cretaceous–Paleogene (K–Pg) mass extinction, diversity in the ginkgo-lineage was probably already much reduced (Crane, 2013).
Ginkgo survived the K–Pg extinction in both the northern and southern hemispheres. However, the last record of ginkgo from the southern hemisphere was soon after, around 60 Mya, ginkgo remained widespread in the northern hemisphere through most of the Cenozoic (65 Mya to present). During the Early Eocene (56–50 Mya), the warmest phase of the last 65 million years, ginkgo grew at very high northern latitudes, in places such as Spitsbergen, Arctic Canada, and Alaska. Later, as the climate cooled, especially at the beginning of the Oligocene (ca. 34 Mya), ginkgo appears to have been forced into more southerly latitudes but still remained widespread (Crane, 2013).
Climatic cooling and drying during the later Cenozoic seems to have had a major influence on the distribution of ginkgo. In North America, ginkgo is last recorded in the Pacific Northwest about 15 Mya (Wheeler & Dilhoff, 2009), and in Europe around 5 Mya (Kovar-Eder, Givulescu, & Hably, 1994; Kovar-Eder, Kvaček, Martinetto, & Roiron, 2006). It also appears to have been extinguished from Japan around this time (Uemura, 1997). Similar regional extinction is seen in many other trees, but in the case of ginkgo, regional loss very nearly resulted in complete extinction. At the end of the last Ice Age, ginkgo appears to have been scarcely hanging on in scattered locations across eastern and south-central China. By the time modern humans arrived in that part of Asia, perhaps 50,000 years ago, ginkgo was already a relic. The precise reasons for this decline remain a mystery. The ginkgo lineage had proved highly resilient through more than 200 million years of dramatic environmental change. Why it later underwent such a rapid and dramatic decline is the central paradox of the ginkgo life story.
4 ETHNOBOTANY AND CULTURAL BIOGEOGRAPHY
The written record of plant cultivation in China extends back several millennia, but ginkgo does not appear until relatively recently, about 1,000 years ago. In these early records it is referred to as a “nut tree.” In strict botanical parlance, a nut is a hard-walled fruit with a single seed. Ginkgo is different; its hard shell is part of the seed rather than the fruit wall. Nevertheless, the function of the “meat” in ginkgo seeds and the true nuts of other plants is the same: to provide food for the embryonic plant. It was probably this edible nut-like gametophyte that first attracted attention. This was the first step in the remarkable resurgence of ginkgo at the hands of people.
Ginkgo nuts may have been collected from wild trees for thousands of years, but the earliest undisputed historical reference to ginkgo is a famous exchange of poems written during the Song Dynasty in the 11th century. Subsequently ginkgo is mentioned frequently in Chinese literature, especially in the 13th and 14th centuries, as “duck foot,” “silver apricot,” “white eye,” “white fruit,” and the “grandfather–grandchild tree.” Similar names appear later in records from Japan, indicating that, like many other plants, ginkgo was transported by people from China to Japan, probably during the medieval period (Crane, 2013; Hori & Hori, 1997). Japan and Korea are the only places outside China where there are truly ancient living ginkgo trees and where ginkgo is still grown for its nuts.
The long history of ginkgo cultivation in China, combined with millennia of human impact on the Chinese landscape, makes it difficult to determine whether any true native populations of ginkgo remain. Large, and undoubtedly old, ginkgo trees can be found in many Chinese provinces. The latest research into centers of genetic diversity suggests that two potentially native ginkgo populations persist; one inland at Jinfo Mountain, Chongqing Municipality, and one closer to the coast, south of Shanghai at West Tianmu Mountain, Zhejiang Province (Gong, Chen, Dobes, Fu, & Koch, 2008; Gong, Qui, Chen, Ye, & Fu, 2008; Zhao, Paule, Fu, & Koch, 2010).
Ginkgo first attracted the attention of western science in the 1690s when Engelbert Kaempfer, a physician to the Dutch East India Company, was based on the small man-made island of Dejima in Nagasaki Harbor. At that time, Dejima was the sole trading point between Japan and the outside world, and although Kaempfer's movements on the mainland were greatly restricted, ginkgo was among the plants he encountered. On his return to Europe, Kaempfer published the first western description and illustration of ginkgo in his Amoenitatum Exoticarum in 1712. Kaempfer (1712) was also the first to use the name “ginkgo,” which derives from the regional Kyushu pronunciation of the Japanese kanji for this tree (Nagata, DuVal, & Crane, 2015).
The first living ginkgo trees introduced to Europe probably arrived, either as seed, seedlings or cuttings, around 1730–1750, perhaps from Japan, but equally likely from China and Korea. Two old trees in the low countries of Europe are thought to date from this time. By the 1760s, ginkgo was being grown in Britain, and by the 1780s it had crossed the Atlantic and was being cultivated outside Philadelphia. Ginkgo was not mentioned by Carl Linnaeus in Species Plantarum (Linnaeus, 1753), but it was eventually named in 1771 after Linnaeus received a specimen from the British nurseryman, James Gordon. Gordon most likely sent Linnaeus a young ginkgo plant, judging from Linnaeus’ herbarium specimen, now in the collection of the Linnean Society of London. On young plants, extension shoots predominate and these produce leaves with a deeply divided lamina (Figure 1b). This most likely accounts for “biloba,” the specific epithet that Linnaeus chose.
5 CULTURAL SIGNIFICANCE
Human attraction to the edible ginkgo “nut” was likely critical to the early survival of ginkgo in landscapes dominated by people. When the smelly, fleshy seed coat is removed, the hard sclerotesta resembles a pistachio nut and the developing gametophyte inside can be boiled, roasted or stir-fried. Ginkgo seeds are used in sweet and savory dishes of all kinds in Chinese, Japanese, and Korean cuisine (Figure 2b,c).
Ginkgo is also widely used as a herbal medicine. Extracts from its leaves are a popular dietary supplement in Europe (and increasingly in North America) for the enhancement of cognitive function. This appears to be a new kind of medicinal use that originated in Europe (Crane, 2013). It is the seeds, rather than the leaves, that are used more commonly in traditional Chinese medicine (Gold, Cahill, & Wenkin, 2002; Gold, Cahill, & Wenkin, 2003; York, 2006).
In parallel with its culinary and medicinal uses in eastern cultures, ginkgo with its distinctive leaves and great longevity, has also taken on symbolic meaning in Buddhism, Daoism, and Confucianism (Figure 3a,b). In Japan, ginkgo also became incorporated in the indigenous religion of Shintoism. Many of the great ginkgo trees of China, Japan, and Korea are in the grounds of Buddhist temples or Shinto shrines. Ginkgo wood has been used to carve religious statues and old ginkgo trees are commonly adorned with inscriptions or ribbons expressing the hopes and prayers of local people (Crane, 2013. Mature ginkgo trees can also develop downward-growing, stalactite-like shoots that are also culturally important, especially in connection with fertility and the nursing of infants. These downward pointing shoots send up sucker shoots when they reach the ground, resulting in a pattern of growth that more closely resembles a thicket than an individual tree (Crane, 2013).
Perhaps through its connection with spirituality, but also through the sheer elegance of its distinctive foliage, and its broader association with eastern cultures, the ginkgo leaf has become a popular motif in western and eastern art. It appears in paintings, jewelry, sculptures and a variety of other cultural objects (Figure 3c,d). Most famously, in the early 19th century ginkgo was the inspiration for a much-loved poem by Johann Wolfgang von Goethe the author and statesman who also founded the science of morphology (Kaplan, 2001). Interested in the ginkgo leaf both for its form and also its symbolic meaning, in his poem “Ginkgo biloba,” presented to Marianne von Willemer his muse and the wife of a close friend in 1815, he asks:
Is it one living being,
That divides itself into itself
Are there two who have chosen each other,
So that they are known as one?
(Unseld, 2003).
Today, ginkgo is encountered most commonly as a street tree. After the fires that followed the great Kanto earthquake in 1923, the Japanese government undertook trials to determine which species of trees to plant. They settled on ginkgo as a tree with some resistance to fire that was also able to thrive in urban environments. From Seoul and Shanghai to Chicago and Berlin, ginkgo is now one of the most widely planted of all street trees (Crane, 2013). Ginkgo is among the most common street trees in Manhattan, and there are almost 60,000 ginkgo trees in the five boroughs of New York City, U.S.A. Horticulturalists have developed many varieties of ginkgo to suit different planting sites and have also selected a surprising variety of leaf forms that range from variegated, to deeply divided, as well as forms in which the leaves do not unfurl correctly and resemble small trumpets (Crane, 2013).
6 GINKGO: AN EXEMPLAR FOR PLANT SPECIES SURVIVAL
The biography of ginkgo is one of the most extraordinary in all the plant kingdom. In the face of dramatic changes on our planet over the past 200 million years ginkgo proved resilient, yet perhaps for the past 15 million years it has been in decline. Natural forces brought it to the brink of extinction and human dominance on our planet could have pushed it into the abyss. Remarkably, unlike many other trees, ginkgo has flourished alongside people and in the past 50 years ginkgo has been resurgent. Interest in growing ginkgo, what it stands for scientifically, and the ways in which it might be useful, has never been higher. A draft of the ginkgo genome is also now available (Guan, 2016).
Almost everywhere that ginkgo grows today it has been taken there by people. Ginkgo reminds us that conservation through cultivation is an important means of protecting threatened plants. There are many other examples: from the Wollemi Pine (Wollemia nobilis) in Australia, to Franklinia (Franklinia alatamaha) in North America, where ex situ conservation has proved important for species survival. Ex situ conservation must not cause us to neglect the conservation of natural habitats, but it is an important tool in helping secure plant diversity for the future. The biggest threat to the future of plant diversity is habitat loss. We neglect at our peril the need to conserve the natural habitats that support individual species, but in an uncertain world it is also important to use all the tools and approaches at our disposal to secure the variety of plant life.
ACKNOWLEDGMENTS
I thank the Organizing Committee of the XIX International Botanical Congress, 2017, in Shenzhen for the invitation to present a public lecture on ginkgo, and the editors and staff of Plants, People, Planet for their assistance in preparing this summary of the lecture, including elements from Crane (2013), for publication.
