Ginkgophytes
Maidenhair trees
The genus Ginkgo, represented today by the widely-cultivated Chinese species Ginkgo biloba, has an evolutionary lineage that dates back to the Jurassic, and the group probably dates back to the Permian. Ginkgoes were very successful during the Jurassic and Early Cretaceous, but started to decline in diversity in the Late Cretaceous with the advent of angiosperms. By the Paleocene, diversity in the genus Ginkgo was reduced to a single polymorphic species, often referred to as Ginkgo adiantoides, which produced leaves virtually indistinguishable from modern-day Ginkgo biloba. This species was mainly distributed in the northern regions due to the tropical environment at that time. As the Earth's climate cooled during the Oligocene, the species took on a more southerly distribution than it had occupied previously. In addition, the number of fossil sites decreases sharply. Approximately seven million years ago it disappeared from the fossil record of North America.
Ginkgo adiantoides was particularly abundant in Europe at the start of the Pliocene, but disappeared from that region by about 2.5 million years ago. There are very limited numbers of fossils found from the Pliocene, and for the Pleistocene, no fossils of Ginkgo are known. Western scientists thought that Ginkgo had become extinct, but it managed to survive in China until modern times. Ginkgo were mainly found in monasteries in the mountains, where they were cultivated by Buddhist monks. The Ginkgo was brought out of these mountains by approximately 1,100 AD and spread quickly throughout temperate Asia. It was first planted in Europe in the early 1700's and in America later that century. It now is a common street tree throughout North America and Europe due to its adaptability to urban environments.
Ecology & Form
Stems
Conifer-like architecture and form, but trees take on an angiosperm-like silhouette when older
Ginkgoes are woody trees, exhibiting a eustele with cambium
They are easily identifiable in the winter due to their distinct long-shoot and short-shoot morphology
Long shoots are normal-looking twigs, with pycnoxylic wood
Short shoots are stunted branches, with manoxylic wood
Ginkgo can sprout from buds near the base of the trunk (lignotubers) in response to disturbances (e.g. soil erosion)
This clonal growth of Ginkgo indicates a strategy for survival in disturbed streamside environments
Fossil sites from the Late Cretaceous and Cenozoic indicate that Ginkgo was largely confined to disturbed streamside and levee environments (Royer et al. 2003)
"...the life-history traits of Ginkgo (e.g., slow growth rate, late reproductive maturity, extended reproductive cycle, large and complex seeds, large and slowly developing embryos) are counter to those considered advantageous in modern disturbed habitats"
Leaves
Ginkgo biloba, as well as some extinct members such as G. adiantoides † and G. gardneri †, possess(ed) fan-shaped leaves
Shape highly variable
Long shoot leaves tend to be bilobed; short shoot leaves tend to be fan-shaped
Leaves are deciduous turning a bright color during autumn. An early frost tends to make most of the leaves fall off at once.
The veins in the leaves display open isotomous branching
The Basidiomycete fungus, Bartheletia paradox, grows exclusively on fallen Ginkgo leaves
Roots
Older individuals can produce aerial roots on the undersides of large branches in response to disturbances (e.g. crown damage), which can lead to clonal trees
Reproductive Structures
Ginkgo biloba is dioecious (i.e. separate male and female trees)
Male
Pollen produced in "simple" cones (=microstrobili) on short shoots
Pollen sacs (microsporangia) connected to sporophylls on a central axis
Sperm are large, flagellated, zoidogamous (sperm swim to egg)
Female
Paired ovules / seeds born on stalks on short shoots
Ovule has a three-layered integument
Pulpy outer layer (sarcotesta) making the seed appear fruit-like
This layer produces butryic acid which gives the seeds a disagreeable odor
N.B. Ginkgo is a gymnosperm and does not produce fruit!
Stony inner layer (sclerotesta) creating a pit-like layer in the seed
Thin endotesta
Ancient Dispersal Agents: A long-tailed bird (Jeholornis sp.) from the Early Cretaceous found with a large number of ginkgo-like seeds in its crop.
This provides direct evidence that early birds potentially could have been involved in seed dispersal activities, although the seeds’ intact nature suggests they were destined for digestion in the gizzard. In general, Ginkgo biloba seeds do not fit the typical profile of a fruit dispersed by modern birds (van der Pijl 1982).
Most speculation about Cretaceous ginkgo dispersal agents centered on dinosaurs, based primarily on their temporal overlap.
If dinosaurs were involved with the dispersal of ginkgo seeds, it probably would have been carrion feeding scavengers, with teeth adapted to tearing and swallowing flesh, rather than herbivores with grinding dentition that would have crushed the thin-shelled seeds.
At any rate, any connection between dinosaurs and ginkgo seed dispersal is, at best, conjecture based on circumstantial evidence.
Above: Leaves of Ginkgo, showing the bilobed morphology of long shoot leaves
Classification
└Ginkgophytes
Diversity
Maximum diversity in Jurassic and Early Cretaceous, with a decline during Late Cretaceous and Cenozoic
The genus Ginkgo dates back to the Middle Jurassic
By the Paleocene, Ginkgo adiantoides was the only species left in the Northern Hemisphere
One extant species, Ginkgo biloba
Baiera †
Braun 1843; Florin 1936
Permian to the Cretaceous, worldwide.
Fan-shaped petiolate leaves that are deeply lobed into four segments, deeply incised into slender segments
B. africana
B. darleyensis
B. digitata
B. gracilis
B. mansfeldensis
B. muensteriana
Eretmophyllum †
Thomas 1913
Middle Jurassic of England, Norway, Afghanistan, Italy, Kazakhstan, Uzbekistan, Japan, Georgia, Siberia, Mongolia, France, China, and Czech Republic
Leaf simple, large, coriaceous, entire-margined, oblong to oblanceolate, tapering gradually at the base to a short and thick cuneate petiole; apex retuse, rounded or sometimes asymmetrical. Two veins are present at the base, dichotomously branching several times in narrow angles; veins in the middle portion of the leaf parallel, then converging toward the apex. Resin bodies absent.
Leaf amphistomatic. Both the upper and lower epidermis comprising alternating stomatal and non-stomatal bands; lower epidermis possessing wider non-stomatal bands and higher stomatal density. Stomata complex haplocheilic, monocyclic or incompletely dicyclic; guard cells sunken, surrounded by four to six subsidiary cells. Free and undeveloped papillae present on subsidiary cells. Stomatal apertures are randomly oriented.
E. neimengguensis (Li et al. 2017)
E. pubescens (Thomas)
E. saihanense (Seward)
Ginkgo
Linnaeus 1771,
G. adiantoides †
G. apoda †
G. biloba (only living species)
G. gardneri †
G. yimaensis †
Ginkgodium nathorsti †
Yokoyama 1889
Ginkgoites †
Seward 1919
Late Triassic - Paleocene of Brazil and Alberta
Ginkgoites is a genus that refers to extinct plants belonging to Ginkgoaceae. Fossils of these plants have been found around the globe during the Triassic, Jurassic, Cretaceous, and Paleocene-age Porcupine Hills Formation in Alberta. The name was created as a form genus in 1919 by Albert Seward who stated: "I ... propose to employ the name Ginkgoites for leaves that it is believed belong either to plants generically identical with Ginkgo or to very closely allied types".[1]
G. huttoni †
G. acosmia †
G. antartica †
G. australis †
G. myrioneurus †
G. pluripartita †
G. obrutschewii †
G. tigrensis †
G. troedssonii †
Ginkgoitocladus †
Krassilov 1972
Karkenia henanensis †
Krassilov 1972
Jurassic - Early Cretaceous of China
Ovulate organs consisting of a peduncle and helically arranged, up to about 100 small, orthotropous but incurved ovules; pedicel present; nucellus largely free
Unlike other ginkgoales, the seeds are borne on cone-like aggregations
Ovuluate organs of Karkenia are associated with leaves of the Ginkgoites, Sphenobaiera and Eretmophyllum types
Nehvizdyella bipartita †
Compound ovuliferous reproductive organ consisting of a main axis and two short secondary axes, each terminated by a large cupule-like structure. Each cupuleencloses one orthotropous ovule. Seeds consist of sclerotesta and sarcotesta.
Pseudotorellia nordenskioeldii †
Florin 1936
The leaves are linear to the lanceolate or obovate, straight or somewhat falcate, and gradually narrowing towards base; the apex is obtuse, rounded, or acute
Two veins enter the leaf, dichotomize several times closer to the base, run parallel in the middle of the leaf, and disappear before the apex
Resin ducts are sometimes observable between veins.
The stomatal topography on the lower surface is diverse: sparse solitary stomata throughout the entire surface, stomata forming discontinuous rows, or stomata arranged in stomatal bands, located between the veins.
The density of stomata in bands varies considerably; stomata are orientated longitudinally, more seldom obliquely, without distinct orientation near the apex.
The stomata are monocyclic to incompletely amphicyclic
The guard cells are sunken, wing-like, or crescent-shaped, often with long polar projections.
The subsidiary cells 4–7 (10) are with or without papillae
The anticlinal walls are straight or wavy
Sphenobaiera ikorfatensis †
Florin 1936; Harris & Millington 1974
Leaf as a whole more or less broadly wedge-shaped, without a distinct petiole
Lamina forking one or more times to give segments
Veins forking repeatedly, several in a segment, nearly parallel and ending separately in the distal margin
Cuticle well developed (of Ginkgoalean-type) with stomata scattered or in broad bands, stomata sunken and surrounded by several haplocheilic subsidiary cells.
Toretzia longifolia †
Stanislavsky 1973
Trichopitys heteromorpha †
Meyen 1984
Permian of southern France
Stems lack short-shoot, long-shoot morphology as in other Ginkgoales
The leaves are arranged in a spiral on long stems. The leaves are not flattened and they do not have a differentiated petiole. They are up to 10 cm long and are divided into four to eight segments.
When the vegetative stems are formed, they produce the fertile shoots in the axils of the leaves and have an inconspicuous axis. The axis carries two to six branches arranged in a spiral, each of which carries an ovule curved backwards. The ovules are small, about 6 mm long, flattened, orthotopic, and inverted. The female axes which carry the seeds resemble morphologically abnormal male axes, as can occur in Ginkgo.
If Trichopitys is a ginkgophyte, it would be the earliest member of the group
Umaltolepis mongoliensis †
Krassilov 1972; Herrera et al. 2017
These reproductive structures resemble those in Peltasperms or Corystosperms, but bear ginkgophyte foliage
Woody plant with long and short shoots; short shoots with alternating pseudowhorls of persistent bud scales and persistent leaf bases
Short shoots generally branched, commonly with a seed-bearing structure near the tip
Seedbearing structure is a radially symmetrical cupule borne on a short stalk that expands into a prominent flange just below the cupule base
Cupule consisting of a slender central column bearing an umbrella-like, four-lobed covering at the apex
Each cupule lobe thick, resinous, and with a thick outer cuticle
Cupule lobes extending downward to clasp the central column just above the level of the flange
Near its tip, just below where the cupule covering is attached, the column is
four-angled and bears four winged seeds, one along each angle
Each seed is pendulous and entirely covered by one of the cupule lobes
The micropyle of each seed is inside the cupule just above the level of the flange
Yimaia †
Zhou & Zhang 1988
Middle Jurassic of China
Ovulate organs consisting of a peduncle and up to eight or nine terminal, sessile, contiguous, and orthotropous (straight, upright, and with a micropyle at apex) ovules
The ovules are associated with leaves of the Baiera or Ginkgoites type morphology
Y. capituliformis (Zhou et al. 2006)
Y. qinghaiensis (Wu et al. 2006)
Y. recurva (Zhou & Zhang 1988)
Above: Ginkgoites huttoni † from the Middle Jurassic
Above: Baiera gracilis †
Above: Sphenobaiera digitata †
Above: Reconstructions of the leaves and seed-bearing structures of three different extinct ginkgo-like plants discovered and described by Zhou Zhiyan from the Middle Jurassic, about 170 Mya, at the Yima mine in Henan Province, China. Left: Ginkgo yimaensis showing lobed leaves and seeds borne on short stalks; top right: Yimaia recurva showing deeply-lobed leaves with linear leaf segments and seeds borne in clusters; bottom right: Karkenia henanensis showing deeply-lobed leaves with linear leaf segments and seeds borne in elongated, cone-like, aggregations. Photographs: Peter Crane. Drawing (c) by Pollyanna von Knorring (From Crane 2018, Fig. 1)
Above: Reconstruction of Trichopitys heteromorpha
Above: Nehvizdyella bipartita † (from Fig 39, Kvacek et al. 2005)
Above: Reconstruction of Umaltolepis mongoliensis and attached Pseudotorellia resinosa leaves (from Fig 4, Herrera et al. 2017)
Above: Ginkgo gardneri †
Above: Ginkgo adantoides †
Above: Reconstruction of Baiera †
Above: Reconstruction of Ginkgo apoda †
Above: Reconstruction of Ginkgo adantoides †
Additional Reading
Fossil relative from the Early Cretaceous