Review of Palaeobotany and Palynology 158 (2009) 1–13
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Review of Palaeobotany and Palynology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / r ev p a l b o
The Neogene flora from Badaogou of Changbai, NE China — Most similar living
relatives of selected taxa and relations to the European record
Johanna Kovar-Eder a,⁎, Ge Sun b,c
a
b
c
State Museum of Natural History Stuttgart, Rosenstein 1, 70191 Stuttgart, Germany
Palaeontological Institute, Shenyang Normal University, 253, North Huanghe Street, Shenyang 110034, China
Research Center of Paleontology, Jilin University, 6, Ximizhu Street, Changchun 130026, China
a r t i c l e
i n f o
Article history:
Received 12 March 2009
Received in revised form 13 July 2009
Accepted 19 July 2009
Available online 28 July 2009
Keywords:
Cuticles
Leaves
Morphology
Systematics
Neogene
a b s t r a c t
The diatomites exposed in the surroundings of Badaogou town, in the counties of Linjiang and Changbai, Jilin
Province of China, bear a rich Neogene leaf assemblage. Previously, the most similar living relatives (MSLRs)
of Sassafras paratsumu Chen (Lauraceae), Acer rotundatum Huzioka (Sapindaceae, subfam. Aceroideae, sect.
Platanoidea), and A. trifoliatum Geng (Sapindaceae, subfam. Aceroideae, sect. Trifoliata) have been
determined based solely on gross morphology. Cuticle preservation in the plant material from Badaogou
allows the comparison of epidermal features. Thus, Sassafras tzumu (Hemsley) Hemsley is confirmed as the
unambiguous MSLR of S. paratsumu.
The cuticular features of Acer rotundatum best match A. mono Maximowicz and A. cappadocicum Gleditsch.
Only the stoma and aperture length are slightly shorter in A. mono than in A. cappadocicum, therefore more
closely resembling A. rotundatum.
Based on gross morphology, earlier workers already regarded A. triflorum Komarov as the MSLR of Acer
trifoliatum. The cuticle, however, bears some differences. In A. trifoliatum the stomata are slightly bigger, the
adaxial surface is only faintly, if at all, striate, and the anticlinal walls are straight; in A. triflorum, however,
the anticlinal walls are undulate and the surface shows distinct striation. Compared to other East Asian
members of sect. Trifoliata – A. griseum (Franchet) Pax, A. mandshuricum Maximowicz, and A.
maximowiczianum Miquel – the combination of features match best with A. triflorum. This includes leaflet
shape and size, trichome bases of simple, filiform trichomes girdled by roundish cells, and the presence of
uniserial, short-celled, glandular trichomes in intercostal areas abaxially.
The modern counterparts of the fossil taxa are elements of the modern flora of China.
© 2009 Elsevier B.V. All rights reserved.
1. Introduction
The Eurasian Neogene plant record has received unequal attention.
Though not fully understood, European floristic change and vegetation development are rather well known while the data from Asia are
spotty, except for the rich Japanese record. Neogene plant occurrences
have been recorded in NE Asia, in the Russian Far East, China, Japan,
and Korea. They are of increasing interest for our improved understanding of the global floristic, vegetation and climate evolution. Plant
systematic investigations, however, have been restricted largely to
gross morphology, with cuticular studies remaining an exception. Due
to its diversity, the flora of Shanwang (Shandong Province, Miocene)
is the most famous among the Neogene Chinese record, e.g. Hu and
Chaney (1940).
⁎ Corresponding author. Fax: +49 711 8936 100.
E-mail address: [email protected] (J. Kovar-Eder).
0034-6667/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.revpalbo.2009.07.005
Plant remains from the Ma'anshancun formation of the Badaogou
area in the Changbai Shan, Changbai County, Jilin Province (Fig. 1),
were firstly mentioned in the Palaeontological Atlas of Northeast
China (1980). By the Geological Bureau of Jilin (1988) a drill core
through the Ma'anshancun Formation from Ma´anshan village of
Badaogou town was described. This profile (Table 1) shows
interbedding basalts and terrestrial sediments. The following foliage
taxa have been listed there: Acer subpictum, Betula mioluminifera,
Betula sp., Carpinus miofangiana, Carpinus sp., Juglans cf. miocathayensis, Quercus cf. grandidentata, Q. cf. furuhjelmi, Salix, Tilia
miohenryana, Trapa sp., Ulmus, Zelkova, as well as diatoms Melosira,
and Cyclotella (Li 1969).
Since 2002, the flora from the diatomite in the surroundings of
Badaogou, about 120 km west of Changbai town, has been sampled by
the staff of the Research Center of Palaeontology and Stratigraphy
(RCPS), Jilin University, China. In 2006 a field trip organized by the
authors within the frame of project CZ295 of the Sino-German Center
of Science Promotion led, besides other destinations, also to
Badaogou. The section was demonstrated and samples were taken
for pollen analysis; some leaf remains were also collected. First cuticle
2
J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
Fig. 1. Geographical setting.
preparations were very successful, prompting detailed cuticular
studies. In 2007 a joint Sino-German field trip visited this site again.
It took the profile, collected basalt samples for dating and collected
further plant remains. In 2008 further material was collected by the
staff of the RCPS.
The assemblage turned out to be species diverse. It predominantly
includes deciduous woody angiosperm taxa of the following families
Berberidaceae (?), Betulaceae, Ericaceae, Fagaceae, Juglandaceae,
Lauraceae, Rosaceae, Sapindaceae, Salicaceae (?), Tiliaceae, Ulmaceae,
and a few conifers (Pinaceae, Cupressaceae). Currently, more than 20
taxa have been roughly identified based on foliage. Most taxa are
deciduous; roburoid oak foliage is most common. The geological
setting – diatomites intercalating with eruptive deposits – along with
the zonal taxa prevailing over intrazonal ones indicate “volcanic
floras” sensu Kvaček and Walther (2001): they are usually more
relevant for palaeoclimatic reconstruction than near-shore and
basinal lowland floras. First investigations of the pollen record and
diatoms show very good preservation and high diversity (Kovar-Eder
et al., 2006, 2007; Stachura-Suchoples et al., 2008).
The most similar living relatives (MSLRs) of fossil taxa are highly
relevant to determine the ecological and climatological implications
of the fossil record. Consequently, the firm determination of MSLRs is
crucial for high-quality reconstruction and modelling. So far, MSLRs
for most Neogene leaf taxa from China have been proposed based
solely on gross morphological comparisons. The present results
focused on Sassafras and two maples confirm the MSLRs based also
on cuticular morphology.
2. Geographical setting and geology
The Changbai Shan (Changbai Mountains) stretch along the border
region between China and North Korea (Fig. 1). They originated from
Oligocene (28.4 Ma) volcanism that increased during Miocene and
Pliocene times, lasting until the Pleistocene (1.2 Ma) (Geological
Bureau of Jilin, 1988). The highest elevation is the Baitou Shan
(2744 m), which has a maar lake on top. The widespread Neogene
volcanism in this region is related to the collision of the Pacific plate
with the Eurasian plate. This led to the formation of numerous
Miocene and Pliocene sedimentary basins and the gradual opening of
the Japan Sea. The famous diatomite fossillagerstaette from Shanwang
(Shandong Province) is situated in one of these basins. There, basal
beds have been dated to 18 Ma (Deng et al., 2003; Wang and Deng,
2005), and basalts intercalating with the plant-bearing strata indicate
15.517 Ma (Yang and Yang, 1994).
In Changbai County and its neighbouring areas of eastern Jilin and
northeastern Liaoning provinces, the fossil-bearing strata with
diatomites are named Ma'anshancun Formation. In Changbai County,
the Ma'anshancun Formation covers an area of about 150 km2.
Diatomite is mined in the villages Ma'anshan, Xidape, Qidaogou and
Shiqidaogo at an elevation of about 700–800 m altitude. In Ma'anshan,
Xidape and Qidaogou, the diatomites yield abundant plant remains.
Badaogou town is situated at the bank of river no. 8 near the river
mouth into Yalu river, which marks the border to North Korea. The
plant remains investigated were collected from the mine Xidape
(41,54° N, 27,31° E) near Badaogou.
Stratigraphically, the Ma'anshancun Formation consists of two
members (Table 1). The Lower Member is composed of sandstones
and silty clays intercalating with basalts and diatomites. The Upper
Member consists of sandstones and silty clays intercalating with
diatomites and diatomitic clay. The Ma'anshancun formation has a
thickness of 142 m. It unconformably overlies Proterozoic strata and is
overlain by the Pliocene Chuandishan Formation, which is composed
of basalts. Due to weathering, the soft diatomites are not exposed at
the surface and can only be studied inside the mining tunnels.
About 150 m west from the mine Xidape, a small stream bed is
developed where three basalt levels crop out. The lowermost is at
least 20 m thick. The superimposed, not well-exposed sediments are
about 5 m thick. The overlying basalt is about 10 m thick and is
followed by 8–10 m of again not well-exposed sediments. The
uppermost, thick basalt already belongs to the Chuandishan Formation. The plant remains studied derive from the diatomites below the
uppermost basalt sheet, i.e. from the top of the Ma'anshancun
Formation. Based on the profile of the drill core at Ma' anshan village,
we are probably dealing with the Upper Member developed directly
above the olivine basalt sheet, which has been dated by Ar/Ar isotopes
(Table 1, level 11) (Geological Bureau of Jilin, 1988).
Table 1
Lithological sequence of the drill core at Ma´anshan village of Badaogou town
(Geological Bureau of Jilin, 1988).
Overlying: Pliocene Chuandishan Formation (basalt)
―unconformity―
Ma'anshancun Formation
Upper
21.
20.
19.
18.
17.
16.
15.
14.
13.
12.
Lower
11.
10.
9.
8.
7.
6.
5.
4.
Member
Yellow and grey sandstone
Yellowish-red silty clay
Greyish-green, silty diatomite
White diatomite
White-green diatomite, diagonal bedding
Greyish-white diatomite with clay
Yellowish-white foliate diatomite and sandstone
Grey-green diatomite
Greyish-white lutaceous siltstone, with diatomite
Yellow siltstone
Member
Greyish-black olivine basalt
Yellow, middle-fine sandstone
Greyish-black diatomite, with silt
Greyish-white diatomite
Buff sandstone
Yellow, fine sandstone
Greyish-white lutaceous siltstone
Greyish-black olivine basalt, with plagioclase porphyritic
crystal
3.
Greyish-white silty diatomite with plant fossils
2.
Greyish-green silty clay
1.
Greyish-green, lutaceous siltstone , with gravels
―Unconformity―
Underlying: Proterozoic strata
( thickness in m)
1.9
2.3
0.3
0.4
4.3
2.7
0.5
1.9
0.9
1.0
7.1
0.9
0.6
0.4
5.0
3.4
7.2
19.6
15.4
14.4
8.9
J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
The tunnel of Xidape mine enters the slope almost horizontally.
Investigating the diatomite in situ reveals that it is at least partly finely
laminated, possibly representing varves. We collected foliage and
fruits from freshly mined sediment.
3. Age
Ar/Ar dating of the basalt in the upper part of the Lower Member of
the Ma'anshancun Formation (Table 1, level 11) indicates an age of
13.4 Ma (Geological Bureau of Jilin, 1988). However, other basalt
datings from the Lower Member indicate 16 Ma or an even older age
(pers. comm. Prof. Peng, Y.J.). First investigations of the diatom
assemblage of the plant-bearing diatomite showed that the Pliocaenicus cathayanus Wang and P. jilinensis Wang species complex, which
is known so far only from the upper Miocene/Pliocene, is common
there (Stachura-Suchoples et al., 2008). To improve the stratigraphic
framework, basalt samples were taken during the field work in 2007
from the basalts under- and overlying the plant-bearing diatomites
next to the Xidape mine. Processing the samples for Ar/Ar dating is
still in progress (pers. comm. Prof. Wang, P.J.).
4. Materials and methods
The plant material is preserved as carbonized compressions.
Unfortunately, rapid drying causes fragmentation of the foliage.
Therefore, to the extent possible, the material was photographed
directly in the field or immediately after collecting. Cuticle preparations were performed using Schulze's reagents followed by 5% KOH
treatment. The cuticles were then stained by safranin and embedded
in glycerol. Finally, the cover glasses were sealed with nail polish.
Photographs were made using a Leitz interference contrast microscope. The descriptive terminology follows Wing et al. (1999) for
gross morphology, Dilcher (1974) for stomatal complexes and
Metcalfe and Chalk (1979) for trichome bases. For cuticle descriptions,
representative values were obtained by measuring at least three
leaves per taxon, if possible, and taking ten measurements of every
cell type, i.e. stomata, non-modified cells, trichome bases.
All specimens are kept in the RCPS, Jilin University, Changchun.
The cuticular slides are partly kept in the institute in Changchun and
in the State Museum of Natural History in Stuttgart.
The numbering in the collection in Changchun is inconsistent, e.g.
Cb or Cbm for Changbai followed by the year, e.g. 2 or 02, followed by
a dash and the final specimen number, e.g. Cb02-5 or Cb06-001. For
unification reasons, we write Cb followed by the year, e.g., 03, dash,
final number neglecting leading zeros (i.e. instead of Cbm03-002 we
cite Cb03-2).
5. Systematics
5.1. Lauraceae
Sassafras Trew
Sassafras paratsumu Chen
Plate I
1978 Sassafras paratsumu Chen sp. nov. - Acad. Sinica. Cenozoic
plants of China, p. 27, pl. 13 fig. 2, textfig. 12.
1999 Sassafras shanwangensis sp. nov. Trew, - Sun, p. 25, pl. 3 fig. 3.
Material: trilobed foliage nos Cb01-10, Cb03-1.
Macromorphology: trilobed entire-margined leaves; specimen no.
Cb03-1 is an almost complete compression; lobes similar in length,
l = 135 mm, b = 91 mm (widest distance between lobe apices),
laminar shape obovate, symmetrical, petiolar attachment marginal,
base concave/decurrent, base angle acute, apex angle odd-lobed
obtuse, sinus between lobes rounded, apex shape of the single lobes
convex, terminally somewhat pointed, apex angle of the single lobes
3
acute, primary veins suprabasal acrodromous, further order venation
not preserved.
Specimen no. Cb01-10 fragment of an impression; l = 59 mm long
(completed at least 110 mm), b = 83 mm (completed about 113 mm);
base and apex missing; sinus between lobes rounded; primary veins
entering the lobes, secondary veins brochidodromous, intersecondary
veins present, tertiary veins partly opposite percurrent with sinuous
course, partly alternate percurrent or even reticulate, angle of tertiary
veins to primaries inconsistent, from almost perpendicular to slightly
acute and somewhat obtuse, fourth order venation (alternate)
percurrent to reticulate, fifth order venation regular reticulate, areoles
well developed, no details within the areolation discernable. Marginal
ultimate venation looped, near the center of the sinus a fimbrial vein is
developed that continues at both sides of the sinus as an intramarginal
vein, with secondary and tertiary veins joining it.
Micromorphology: cuticle obtained from specimen no. Cb03-1,
both surfaces very delicate, only tiny fragments available, especially
along veins globular secretory bodies preserved; faint cuticular
striation above veins developed, simple, raised trichome bases
scattered, above veins more common than in intercostal areas,
volcano-shaped, trichome base margins thickened, trichome pore 5–
11 (average 8) µm in diameter; adaxial surface: anticlinal walls
weakly undulate, with knob-like thickenings, non-modified epidermal cells 19–32 (average 24) µm in diameter, trichome bases as
described above; abaxial surface: cuticle fragments even tinier and
thinner than those of the adaxial surface; only fragments with one or
maximum two stomatal complexes preserved; non-modified cells
dome-shaped, size of non-modified epidermal cells not well visible,
about 20–27 µm in diameter (only three measured), anticlinal walls
somewhat curved, stomatal complexes paracytic and rhomboidal,
stoma length 12–19 (average 15) µm, width 20–21 (average 20) µm,
length/width ratio 0.6–1, average 0.8, aperture length 7–14 (average
10) µm, trichome bases as described above.
Discussion: The single trilobate leaf compression (no. Cb03-1)
yields the cuticle but does not show venation details, while
fragment no. Cb01-10 lacks cuticle preservation but shows detailed
venation characters. Based on the combination of features (trilobate
leaf shape, paracytic stomatal complexes, secretory bodies, shape of
trichome bases) these leaves are assigned to the Lauraceae and
further to S. paratsumu. Based on gross morphology, S. paratsumu
was compared to S. tzumu (Academia Sinica, 1978. Fossil plants of
China). Since the cuticular features of this fossil taxon are now
available, different Lauraceae with trilobate foliage were compared
here (see Reference material): Sassafras albidum Nuttall Nees,
Sassafras tzumu (a single leaf fragment was available), Lindera
obtusiloba Blume, and L. triloba Blume (synonym Parabenzoin
trilobum (Siebold et Zuccarini) Nakai). S. randaiense (Hayata)
Rehder was not available but the description of Imkhanitskaya
(1966) served for comparison here. L. obtusiloba differs by the basal
acrodromous venation; the lobes are wider and the lateral ones are
distinctly shorter than the central lobe. In L. triloba the venation
is suprabasal acrodromous, but the lobes are of rather acuminate
shape with a distinctly acuminate apex and a sinuous course of
the margin along the lobal sinus, thus differing from the fossils.
Sassafras albidum closely resembles the fossil specimens in gross
morphology by its suprabasal acrodromous venation, lobe shape
and details of the marginal venation.
Regarding micromorphology (Table 2), the stomata in Lindera
obtusiloba, L. triloba and Sassafras albidum are distinctly longer but
less wide, yielding a length/width ratio of 0.9 at minimum. The nonmodified epidermal cells are very big, up to more than 60 µm in
diameter; their thick anticlinal walls partly show a very distinct zigzag
pattern. Scattered trichome bases have been observed in Sassafras
albidum. S. randaiense resembles S. paratsumu in the dome-shaped
non-modified epidermal cells on the abaxial surface, but the stomata
are bigger (Imkhanitskaya, 1966).
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J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
Plate I. Sassafras paratsumu Chen.
1.
2.
3–8.
3–6 .
4.
5.
6.
7, 8.
7.
8.
Cb03-1 compression. Scale bar 1 cm.
Cb01-10 impression. Scale bar 1 cm.
Cuticular structures of the fossil Sassafras paratsumu Chen and the modern S. tzumu (Hemsl.) Hemsl. Scale bar 50 µm.
S. paratsumu, Cb03-1, 3 A-C - small cuticle fragments with single paracytic stomata, and in A and C with dome-shaped non-modified epidermal cells.
Globoid secretory bodies in the mesophyll and a simple trichome base (arrow) situated above a vein.
Adaxial cuticle near the leaf margin, a simple trichome base situated near the margin.
Adaxial cuticle.
S. tzumu.
Abaxial cuticle with dome-shaped non-modified epidermal cells, tiny paracytic stomata and a simple trichome base.
Adaxial cuticle with scattered simple trichome bases.
J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
5
Table 2
Comparison of selected cuticular features of Sassafras paratsumu and modern trilobed Lauraceae species.
Taxon
Stoma Average Stoma Average Ratio stoma
Average Aperture Average Non-modified cells abaxially
length (µm)
width (µm)
length/width (µm)
length
(µm)
(µm)
(µm)
(µm)
Sassafras paratsumu
S. albidum
12–19
18–25
15
21
20–21 20
15–22 17
S. randaiense
(Imkhanitskaya, 1966)
S. tzumu
S. tzumu (Imkhanitskaya,
1966) trilobate leaf
S. tzumu (Imkhanitskaya,
1966) simple leaf
Lindera obtusiloba
19–28
23
19–30 24
14–19
17–22
17
19
16–19 21
17–18 18
14–19
17
14–17 15
20–24
23
L. triloba
17–20
19
0.6–1
0.9–1.6
0.8
1.3
7–14
13–15
10
14
Anticlines slender, curved, cells dome-shaped, diameter 20–27 µm
Anticlines thick, coarsely zig-zag undulate, cells not dome-shaped,
diameter 27–41 µm
Cells dome-shaped, 21–25 × 14–20 µm
0.6–0.9
0.7
6–13
10
Anticlines slender, curved, cells dome-shaped, diameter 16–30 µm
Anticlines sinuate to curved, cells dome-shaped, 17–23 × 8–17 µm
22–23 23
0.9–1.1
1
11–14
13
14–18 15
1–1.4
6–9
8
Anticlines thick, coarsely zig-zag undulate, cells not dome-shaped,
diameter up to at least 64 µm
Anticlines thick, coarsely undulate, cells not dome-shaped,
diameter 27–55 µm
1.2
Closest in micromorphology to the fossil species is Sassafras
tzumu. On the delicate abaxial cuticle the stomata closely resemble
those found in the fossil specimen both in their rhomboidal shape
and their size. The simple trichome bases are scattered abaxially
as well as adaxially. Non-modified epidermal cells bear delicate
anticlinal walls and are dome-shaped in S. tzumu, as in S. paratsumu
(Plate I, 7).
The fossil material from Badaogou also contains two fragments
of entire-margined leaves, one of them, no. Cb06-3, with suprabasal
acrodromous venation. The cuticles are poorly preserved, but
the simple trichome bases, as known in Lauraceae, and the globoid
mesophyllous secretory bodies in specimen no. Cb06-2 point towards
the laurel family. Sassafras is known for its leaf dimorphism and these
remains may well also represent S. paratsumu.
Sassafras ferretianum Massalongo and Scarabelli occurs in the
European Neogene. Its records are rather scanty. The cuticular
features indicate a closer relationship to Sassafras tzumu than to S.
albidum or S. randaiense, e.g. Gerce, Hungary, (Hably and Kvaček,
1997), Vegora, Greece (Kvaček et al., 2002), Auenheim, Alsace, France
(Kvaček et al., 2008).
5.2. Sapindaceae
Acer L.
Section Platanoidea Pax
Acer rotundatum Huzioka 1943
Plates II, III
1940 Acer subpictum auct. non Saporta - Hu and Chaney, p. 61,
pl. 34, figs. 3–5, 7, pl. 35 fig. 1.
1943 Acer rotundatum - Huzioka, p. 129, pl. 24 (4) figs. 1–3, pl. 25 (5)
fig. 2.
1943 Acer subpictum - ibidem, p. 129, pl. 24 (4) figs. 4–6, pl. 25 (5)
fig. 3.
1980 Acer subpictum - Palaeontological Atlas of Northeast China,
p. 333, pl. 208 fig. 5, pl. 210, Fig. 3; non, pl. 202, fig. 4.
1983 Acer rotundatum Huzioka - Tanai, p. 329, pl. 11 fig. 1.
1988 Acer rotundatum Huzioka - Uemura, p. 153.
1999 Acer subpictum Saporta - Sun, pl. 32 fig. 3.
2001 Acer subpictum Saporta - Shang et al., fig. 1/9.
2005 Acer rotundatum Huz. - Pavlyutkin, p. 126, pl. 35 fig. 3 a, pl. 39
fig. 1.
For further extensive synonymy see Tanai (1983, p. 329).
Material: with cuticle preservation nos Cb02-6, Cb06-32, Cb06-82,
Cb06-89, Cb07-119, Cb08-9, Cb08-21, Cb08-55, Cb08-58, Cb08-60,
Cb08-75, Cb08-79; without cuticle preservation: nos Cb03-2, Cb07-1,
Cb07-23.
Macromorphology: foliage palmately quinque-lobate, petiole up to
at least 30 mm long, basally swollen (preserved completely only in
specimen no. Cb07-1); laminar shape round to slightly elliptic, laminar
size micro- to notophyll, central lobe 50–80 mm long, lateral ones
slightly shorter (35 to 70 mm) but only exceptionally preserved
completely, blade width 55–80 mm (measured at the level of the lobe
sinus), leaf base truncate to cordate, angle (wide) obtuse, lobes rather
broad, sinus between lobes rounded (sometimes acute), shape of lobe
apices long acuminate, apex angle acute; margin entire, exceptionally
single large teeth (to smaller lobes) developed, e.g. no. Cb07-1;
venation palinactinodromous, 5 main veins originating at the base,
angle between central vein and adjacent lateral ones 35–45°
(occasionally up to 60°), angle between central vein and basal ones
75–90° (occasionally up to 110°); secondary veins in the free parts
of the lobes brochidodromous, looping in wide arches, sometimes
secondary veins with zig zag course, tertiary veins polygonal
reticulate, areolation formed by quarternaries, well-developed, mostly
four-sided, freely ending veinlets either not well preserved or partly
probably absent, some appear unbranched or one-branched (?).
Micromorphology: ab- and adaxial cuticles delicate; adaxial
cuticle: anticlinal walls only sporadically traceable, curved, surface
distinctly, finely striate, striae densely spaced, running in parallel,
sometimes arranged in star-like bundles; abaxial cuticle: only the
slender oval stomata are visible, stomatal type probably anomocytic,
stomata 11–21(25) (average 14–18) µm long, (7)9–14(17) (average
10–13) µm wide, length/width ratio (0.9)1.1–2.1 (2.7) average 1.2–2,
aperture shape slender slit-like, length 7–10(11) (average 7–8) µm;
two types of trichomes developed (no. Cb08-75), mainly positioned
above thicker veins: (1) simple, filiform, well-staining ones, surface
with longitudinally running, short striae, trichome bases simple,
diameter up to 36 µm, and (2) incompletely preserved, pluricellular
glandular trichomes positioned above rather indistinct and smaller
trichome bases, diameter 16–17 µm.
Discussion: Specimen no. Cb07-1 is the most complete one, but
cuticle preparation was unfortunately not successful. Best preservation of the cuticle is provided in the specimens nos Cb06-82, Cb06-89,
Cb08-75, Cb08-79.
In gross morphology, Acer rotundatum resembles Acer mono
(Tanai 1983) and to a lesser degree Acer cappadocicum. The gross
morphological similarity to A. mono has been described in detail by
Tanai (1983). It comprises the shallowly to deeply 5- to 7-lobed,
entire-margined shape of the blades, the acute to long acuminate
(caudate) lobe apices as well as the quadrangular areolation with
single or lacking freely ending veinlets. Taxonomically, A. mono is
rather difficult due to its wide variability, resulting in numerous
synonyms (van Gelderen et al., 1994). Xu et al. (2008) distinguish it as
Acer pictum subsp. mono (Maximowicz) H. Ohashi. The cuticles of Acer
mono (including A. pictum) and A. cappadocicum are compared here
(Table 3). Generally, both modern species resemble each other very
closely. Comparing the average values, stoma length and aperture
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J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
Plate II. Acer rotundatum Huzioka.
1, 5.
5.
2.
3.
4.
6.
7.
1–7.
8, 9.
8.
9.
10.
8–10.
Cb07-1.
Showing venation details.
Cb03-2.
Cb08-21.
Cb08-79.
Cb08-58.
Cb08-75.
Scale bar 1 cm.
Cb06-82.
Abaxial surface with numerous stomata.
Adaxial surface with striae.
Cb08-75, adaxial surface with striae.
Scale bar 50 µm.
J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
Plate III. Cuticular structures of the fossil Acer rotundatum Huzioka and the modern A. mono Maxim.
1–3.
1, 3.
2.
4–9.
4, 5.
4.
5.
6.
7.
8.
9.
1–9.
Acer rotundatum, Cb08-75.
Abaxial cuticle with stomata and incomplete simple, filiform trichomes.
A pluricellular glandular trichome positioned upon a vein.
Acer mono.
No. 701.
Abaxial cuticle, glabrous, with tiny slender stomata.
Adaxial cuticle with star-likely arranged bundles of striae.
No. 1922, adaxial cuticle.
No. 645, abaxial cuticle with simple trichomes.
No. 2539, two pluricellular, glandular trichomes (arrow) and simple filiform ones above a vein.
No. 1922, abaxial cuticle with one simple, filiform and one globular, pluricellular glandular trichome.
Scale bar 50 µm.
7
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Table 3
Comparison of selected cuticular features of Acer rotundatum and modern compared species of sect. Platanoidea.
Taxon
Stoma length
(µm)
Average
(µm)
Stoma width
(µm)
Average
(µm)
Ratio stoma
length/width
Average
Aperture length
(µm)
Average
(µm)
Acer
Acer
Acer
Acer
Acer
Acer
Acer
(17)18–24(26)
12–23
(18)20–24
16–30
12–21(25)
13–22
13–18
20
17
21
20
16
17
16
(10)12–17(20)
12–20
11–18
11–21
(7)8–17
9–17
11–13
14
15
15
12
12
14
12
1.1–1.7(2.2)
1.5
8–12(15)
10
1.1–1.8
1.4
9–13(14)
11
(0.9)1.1–2.1(2.7)
1.6
6–12
8
6–8
7
mono (measurements of 4 leaves)
mono (Mai and Walther, 1991)
cappadocicum
cappadocicum (Mai and Walther, 1991)
rotundatum (measurements of 4 leaves)
integerrimum (Mai and Walther, 1991)
integerrimum (Ströbitzer-Hermann, 2002)
length are slightly shorter in A. mono than in A. cappadocicum.
In A. rotundatum these parameters are still slightly shorter than in
both the modern species, but they are closer to A. mono than to A.
cappadocicum. In A. mono and A. cappadocicum, two types of trichomes
are developed, mostly upon thicker veins (Plate III, 8, 9): (1) simple
long, unicellular trichomes with longitudinally running short striae
positioned upon large, simple, round trichome bases which appear
sometimes girdled by a ring of short cells and (2) variably shaped
glandular trichomes on smaller, one- to three-celled trichome bases.
Though rare, both trichome types are preserved in the Badaogou
material as well (Plate III, 1–3).
Acer rotundatum is very common in Neogene floras of (North) East
Asia. From numerous sites in China, corresponding foliage usually is still
assigned to A. subpictum Saporta or A. subpictum auct. non Saporta. A.
subpictum, however, is based on fossils from the Pliocene of Cantal in
southern France (de Saporta, 1873). Walther (1972) and, later,
Ströbitzer-Hermann (2002) recognized that A. subpictum is only a
younger synonym of A. integerrimum (Viviani 1833) Massalongo and
Scarabelli, 1859. In our opinion, Tanai (1983) already correctly assigned
fossil foliage from China to A. rotundatum. He also included winged fruits
in this species. As foliage and fruits have never been found attached to
one twig, and because maples are usually species diverse in fossil
assemblages, fruits should be preferably named differently.
Stratigraphically, A. rotundatum is known occasionally from the Early
Miocene and becomes widespread during the Miocene (Tanai 1983).
In the European Neogene, sect. Platanoidea is represented by threelobed A. integrilobum Weber sensu Walther and three- to five-lobed A.
integerrimum (Viviani) Massalongo. Gross morphologically, A. integerrimum differs from A. rotundatum by the straight/attenuate shape of the
lobe apices. The cuticle of A. integerrimum is very difficult to obtain. It was
first recorded by Mai and Walther (1991) and later by StröbitzerHermann (2002). Also, A. integerrimum shares the slender stoma shape
with modern species of sect. Platanoidea and with A. rotundatum. The
small stoma size in A. integerrimum more closely resembles A. rotundatum
than the modern species. While being a rare accessory element in upper
Oligocene to middle Miocene floras, A. integerrimum becomes abundant
only in the late Miocene/Pliocene record, e.g. Massive Central (France,
Roiron, 1991), Willershausen (Germany, Knobloch, 1998).
Most recently, A. integerrimum (a single leaf fragment) has been
described from Auenheim, Alsace (France, Pliocene) (Kvaček et al.,
2008). The authors themselves state the different (broadly oval) shape of
the outer front cavities of the stomata and the absence of adaxial striation
compared to the so far known foliage of A. integerrimum. Further
differences to be added here are the larger and more roundish stomata,
raising more doubts about the specific assignment of this remain.
Section Trifoliata Pax
Acer trifoliatum Geng
Plates IV, V
1978 Acer trifoliatum Geng - Acad. Sinica. Cenozoic plants of China.
p. 129, pl. 105 fig. 5, pl. 110 fig. 1, pl. 111 fig. 6, pl. 112 fig. 5, pl. 113
fig. 1, ill. 64.
1983 Acer trifoliatum Geng - Tanai, p. 341, pl. 17 fig. 4. (figured
from Shanwang).
2005 Acer trifoliatum Cheng - Pavlyutkin, p. 130, pl. 40 figs. 6, 7.
Material: nos Cb02-3 (terminal leaflet); Cb05-6, Cb05-9, Cb05-19
part/counterpart, Cb05-22, Cb06-36, Cb06-74, Cb07-8, Cb07-22,
Cb07-72, Cb08-11, Cb08-63, Cb08-78 (all lateral leaflets).
Macromorphology: leaflets without petiole, probably sessile;
laminar shape ovate to obovate, distinctly asymmetric (probably
lateral leaflets) or petiolate (petiole 5 mm long) and symmetric
(terminal leaflet, no. Cb02-3), leaflet size microphyll, length 46–
50 mm, width 18–25 mm (exceptionally up to at least 86 mm long
and 43 mm wide), length/width ratio 1.8–2.7, base shape convex to
rounded, strongly asymmetric, base angle almost 90° to obtuse, rarely
acute (no. Cb02-3), apex shape acute to slightly acuminate, apex angle
acute, margin with few (up to 3), irregularly spaced large teeth, tooth
apex acute to somewhat rounded, sinus acute, occasionally rounded,
basal side slightly convex, apical side almost straight or slightly
convex; venation: midvein straight to smoothly bent, secondary
venation craspedodromous where the margin is toothed and
brochidodromous where no teeth are developed, spacing of secondary
veins variable between neighbouring ones, 3–10 mm, secondary veins
running smoothly curved and subparallel among each other towards
the margin, some enter the marginal tooth apices, teriaries alternate
percurrent, straight to sinuous, rather densely and regularly spaced,
almost perpendicular to the secondary veins, tertiary veins occasionally in transition to polygonal reticulate (no. Cb06-74), tertiary vein
angle to midvein wide obtuse, quaternary venation and fifth order
veins polygonal reticulate, areolation formed by fifth order veins (nos
Cb02-3, Cb06-74), four- to five- (six-) sided, no freely ending veinlets
(or only occasionally unbranched ones ?) (no. Cb06-74).
Micromorphology: both surfaces delicately cutinized; adaxial
cuticle: rarely preserved, anticlinal walls straight, forming polygonal
cells, size 22–32 µm, average 26 µm, surface faintly striate.
Abaxial cuticle delicate, non-modified epidermal cells partly
somewhat dome-shaped but usually hardly visible, anticlinal walls
straight to somewhat curved, stomatal type and shape of guard cells
unclear, probably anomocytic, only the cuticular ledges of the front
cavities appear distinct, they enclose a more or less wide oval
aperture, the ledges are laterally thickened but very slender at the
poles, so they are sometimes hardly traceable there; length of the
stomatal aperture (9)10–14(17) (average 12–14) µm; two types of
trichome bases occur mainly above veins: 1) one-celled, round, rather
large trichome bases of simple, long hairs, trichome pore girdled by a
ring of sometimes rather large epidermal cells, diameter of the
trichome pore 14–35 µm, average 20 µm; 2) small, more strongly
cutinized trichome bases of uniserial, glandular trichomes, trichome
body built of 3 to 7 short cells, no specific head developed.
Discussion: The laminar shape of most specimens is asymmetric
and therefore they are interpreted as lateral, sessile ones. Only no.
Cb02-3 may be regarded as a terminal leaflet due to the rather
symmetric laminar shape and the presence of a petiolule. In specimen
no. Cb06-74 the areolation details are preserved. In sect. Trifoliata,
freely ending veinlets are mostly lacking or single ones may sometimes be developed (Tanai 1978).
Among all specimens, no. Cb08-72 yielded the best-preserved
cuticle, showing slightly dome-shaped non-modified epidermal cells
J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
9
Plate IV. Acer trifoliatum Geng.
1.
2–6.
2, 3.
3.
4.
5.
6.
1-5.
Cb02-3, terminal leaflet.
Lateral leaflets.
Cb05-22.
Venation details near the base.
Cb08-78.
Cb05-19.
Cb06-74.
Scale bar 1 cm.
and glandular trichomes (Plate V, 1, 2) in addition to stomatal
apertures and large trichome bases, which are preserved in other
specimens as well, e.g. no. Cb05-6 (Plate V, 6). Exceptionally, simple,
long trichomes are preserved in specimens nos Cb06-74 and Cb08-78
(Plate V, 4, 5).
Based on gross morphology, Acer triflorum is regarded to be the
modern counterpart of A. trifoliatum (Tanai 1983). In sect. Trifoliata,
except for A. triflorum, the species A. griseum, A. mandshuricum, and A.
maximowiczianum (syn A. nikoense Maximowicz) gross morphologically resemble A. trifoliatum. In all the modern species the lateral
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Plate V. Cuticular structures of the fossil Acer trifoliatum Geng and the modern A. triflorum Komarov.
1–6.
1, 2.
3.
4, 5.
6.
7.
8, 9.
1–9.
Acer trifoliatum.
Cb08-72, abaxial cuticle with dome-shaped non-modified epidermal cells, stomata and pluricellular, glandular trichomes (arrows).
Cb08-78 abaxial cuticle.
Cb08-78, cuticle submacerated, veins with filiform trichomes.
Cb05-06, trichome bases of filiform trichomes (arrows) above a vein and some stomata.
Cb08-78, adaxial cuticle.
Acer triflorum - abaxial cuticle with dome-shaped non-modified epidermal cells, stomata and pluricellular, glandular trichomes, and in picture 9 a big trichome base of a
simple, filiform trichome above a vein.
Scale bar 50 µm.
J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
11
Table 4
Comparison of selected cuticular features of Acer trifoliatum and the modern compared species of sect. Trifoliata.
Taxon
A. griseum
A. mandshuricum
A. maximowiczianum
A. triflorum
A. trifoliatum
Abaxial cuticle
Adaxial cuticle
Length of stomatal
aperture (µm)
Average
(µm)
Diameter of bases of
simple trichomes (µm)
Average
(µm)
Trichome bases with
girdling cells
Uniserial, glanduliferous
trichomes
8–15
12–17
8–11
(8)9–13
(9)10–14(17)
11
15
10
10
12–14
17–49
13–21
21–59
41–54
14–35
28
18
40
45
20
Present
Absent
Present
Present
Present
Absent
Absent
Absent
Present
Present
leaflets are sessile or nearly so and only the terminal one is
petiolulate. By gross morphology, A. griseum and A. triflorum are
very similar to A. trifoliatum, while in A. maximowiczianum the
leaflet size appears to be somewhat bigger. A. mandshuricum differs
more distinctly by having more slender leaflets and more numerous
but smaller marginal teeth.
The cuticles of A. griseum, A. mandshuricum, A. maximowiczianum
(there as A. nikoense), and A. triflorum have been described in detail
by Ströbitzer-Hermann (2002). These cuticle slides have also been
used for comparison in this study (Table 4). In all species the nonmodified epidermal cells of the abaxial cuticle are more or less domeshaped. The stomatal complexes are probably anomocytic although,
due to only faintly if at all developed anticlinal walls, this feature
remains somewhat obscure. The shape and size of the stomatal
apertures are distinct and therefore offer the best feature for
comparisons. In all species, both fossil and modern, their shape and
size are rather variable within one leaf; nonetheless, all are more or
less wide-oval. In A. griseum, A. maximowiczianum, and A. triflorum
the size of the stomatal apertures is similar. In A. trifoliatum the
stomatal apertures appear to be slightly larger and are even larger
in A. mandshuricum. On the abaxial surface, large trichome bases
encircled by one to two rings of slightly more strongly cutinized cells
occur in A. maximowiczianum and A. triflorum. In A. mandshuricum
much smaller and less characteristic trichome bases were found;
they were confined to major veins. In A. griseum, girdling cells are
less distinct. The fossil A. trifoliatum bears trichome bases encircled
by a ring of roundish, cells (Plate V, 6). The diameters of the trichome
bases are bigger than in A. mandshuricum but possibly do not reach
the largest sizes of A. maximowiczianum and A. triflorum. The most
distinctive cuticular feature, however, is the presence of uniserial,
short-celled, glandular trichomes which occur abundantly in intercostal areas both in A. trifoliatum and A. triflorum. Although A.
griseum, A. mandshuricum, and A. maximowiczianum may sporadically exhibit mainly globular or balloon-shaped, glandular trichomes, they lack the intercostal uniserial structures developed in
A. triflorum and A. trifoliatum. In all compared modern species the
adaxial cuticle shows distinct striation and the anticlinal walls of the
non-modified epidermal cells are undulate. In A. trifoliatum,
however, they are rather straight and the striation is weakly if at
all developed.
From the Miocene of Sichote Alyn (Russian Far East), Akhmetiev
(1973) described A. trifloriformis as a new species based on a single
leaf fragment. This author regards this remain as a leaflet. It is large
(80 × 50 mm), symmetric, and the teeth apices are rather acute. More
remains would be required to confirm the assignment to a maple with
compound foliage.
While the modern members of the sect. Trifoliata are restricted
to Asia, a fossil representative – Acer aegopodifolium (Göppert)
Baikovskaja ex Iljinskaya, recently revised by Walther and Zastawniak
(2005) – is known from the Miocene of Europe. Based on the venation
classification of Tanai (1978), Kovar-Eder (1988) was able to support
the assignment of this maple (designated there as Acer quercifolium
(Göppert) Kovar-Eder) to sect. Trifoliata. In A. negundo L. (sect.
Negundo), which has a similar leaflet shape, freely ending veinlets in
the areoles are well developed and one- or two-branched. Schmitt
Anticlines
Anticlines
Anticlines
Anticlines
Anticlines
undulate, distinctly striate
undulate, distinctly striate
undulate, distinctly striate
undulate, distinctly striate
straight, weakly striate
and Kvaček (1999) were the first to successfully prepare the cuticles
of A. aegopodifolium. They regard A. griseum and A. triflorum as the
closest modern relatives of A. aegopodifolium.
Stratigraphically, A. trifoliatum and A. aegopodifolium do not
appear before the Miocene. The former is restricted to the later early
Miocene of East Asia according to Tanai (1983), while Liu et al.
(1996) indicate an early middle Miocene to Early Pliocene
occurrence. The latter appears in eastern parts of Europe during
the middle Miocene and becomes widespread in the upper middle to
upper Miocene in Central Europe (Kovar-Eder et al., 1994), although
it is usually not abundant.
6. Conclusions and future perspectives
Up to now, cuticular studies of Cenozoic leaf assemblages from
China were rare. The excellent preservation of the foliage from
Badaogou offers a huge potential for taxonomic research and thus
allows inferences on floristic relationships within the northern
hemisphere. This paper presents the results of the investigations on
laurels and maples from Badaogou, but further taxa will be studied.
The future studies on this flora are expected to identify more MSLRs of
the Chinese Neogene plant record.
The MSLRs of Sassafras paratsumu, Acer rotundatum, and
A. trifoliatum have been proposed based on macro-morphological
comparisons prior to this study. For Sassafras paratsumu the cuticular
structures bear unequivocal evidence to confirm the relation to S. tzumu.
In A. rotundatum and A. trifoliatum the cuticle structures are rather
similar to related modern maples. Differential cuticular characters
between the modern species A. mono and A. cappadocicum are minor,
restricted to minimal differences in stoma and aperture length.
These differences, however, point towards A. mono as the MSLR
of A. rotundatum, thus supporting the gross-morphologically based
assumption.
A. trifoliatum is distinctive from modern species of sect. Trifoliata due
to the size of the stomatal aperture, the adaxially straight anticlinal walls
and the faint striation. Nonetheless, the set of features – leaflet shape
and size, large bases of simple, filiform trichomes girdled by a ring of
cells and the presence of uniserial glandular trichomes in intercostal
areas – links this fossil maple closer with A. triflorum than with other
species.
The material investigated here indicates that it should be possible to
calculate the stomatal indices at least of A. rotundatum and A. trifoliatum.
Since the formerly suspected MSLRs have now been confirmed, we can
compare the stomata indices of the fossil taxa to those of their modern
counterparts. Thus, the Badaogou plant assemblage is expected to
provide relevant contributions regarding the atmospheric CO2 concentrations and climate history of Eastern Asia.
7. Reference material
7.1. For Sassafras paratsumu, slides SMNS
Lindera obtusiloba Bl., Mt. Somayama, Prov. Echizen (?), in
montane forest at about 500 m, 18.8.1917, leg. Takenouchi, ex.
Herb. B.
12
J. Kovar-Eder, G. Sun / Review of Palaeobotany and Palynology 158 (2009) 1–13
Parabenzoin trilobum (Siebold and Zucc.) Nakai (=Lindera triloba
Bl.)
Plants of Honshu, 20.9.1984, D.E.Boufford and H. Koyama, No.
23553, Shiga Prefecture: Hira Mountain Range, alt. 350–500 m, ex
Herb. B.
Sassafras albidum Nutt. Nees, Nr. 2175, Arboretum, Bot. Garten
Berlin-Dahlem, 26.10.1962, leg. G.K.Schulze-Menz, ex Herb. B.
Sassafras tzumu (Hemsley) Hemsley, loc. Maoer shan Mt., Anxin
County, Guangxi province. China, coll. Chen Zhaoyu 51296, ex Herb.
KUN.
7.2. For Acer rotundatum, cuticular slides from Ströbitzer-Hermann
(2002), NHMW
Acer cappadocicum, Bot. Gard. Ariamehr, 29.7.1974, Flora of Iran,
No 14271;
Acer fulvescens Rehd., Handel-Mazzetti, Iter sinense 1914–1918,
No. 7914 rev. Acer cappadocicum (Gled.) f. tricaudatum (Rehder)
Rehd. Acqu. 1924, No. 1903;
Acer mono var. marmoratum, leg 2.8.2000, Mt. Fuji, Nishiusuzuka,
Honshu;
Acer mono, No 642, leg. 29.7.2000, Yufutsu Lowland Mire,
Hokkaido;
Acer mono var . mayrii, No. 645, leg. 29.7.2000, Tomakomai
Experiment Forest, Hokkaido;
Acer pictum rev. A. truncatum, syn. A. mono, No 1922;
7.3. For Acer trifoliatum, cuticular slides from Ströbitzer-Hermann 2002,
NHMW
Acer griseum Pax, No 1883; C. China, W. Hupeh; 1883, leg. E.H.
Wilson, det. Camillo Karl Schneider, Acqu. 1907 No. 9765;
Acer mandshuricum Maxim.; Wien, Cult. Hochschule f. Bodenkultur; 5. Juli 1922, leg. K.H.Rechinger, Acqu.1925 No.5016;
Acer nikoense syn. A. maximowiczianum, 26.5.1904, Acqu.1905 No.
6621. (see Ströbitzer-Hermann, pl. 22, Figs 1, 2, 4);
Acer triflorum Kom., Komarov V., Flora Manshuriae, No. 1051;
Fluvium Jalu super, circa Sehi-sida-gou, Manshuria chinensis;
12.7.1897, leg. V. Komarov; Acqu. 1910 No. 8342.
Acknowledgements
We are grateful to the colleagues at the RCPS, Jilin University,
Changchun, and in particular to Prof. Chen Y.J. and Mr. Li C.T. as
well as to Dr. A. Bruch (Frankfurt/Main), Dipl. Biol. V. Wähnert
(Stuttgart) and H. Sommer (Stuttgart) for collecting and assistance
during field work. Prof. P.J. Wang took the basalt samples for dating. Dr.
A. Bruch took samples for pollen analysis. H. Sommer took the photos
of the specimens collected in 2007 directly in the field. Prof. Z.K. Zhou
(Kunming) and Prof. Dr. Z. Kvaček (Prague), Dr. R. Jahn (Berlin), and
Dr. K. Stachura-Suchoples, Potsdam, supported the investigations with
scientific communications and comparative material (herbarium and
cuticular slides). Prof. Dr. H. Walther critically read and commented on
the manuscript. Dr. R. Vogt supported the studies of the first author in
the Herbarium and Botanical Garden Berlin Dahlem. M. Kamenz
(Stuttgart) performed the cuticle preparations. Dong M. (RCPS) helped
the first author in the collection in Changchun and translated relevant
literature from Chinese into English. This work has been performed
within project CZ295 of the Sino-German Center of Science Promotion,
which was initiated by Prof. Dr. V. Mosbrugger and Prof. Dr. Sun G., and
within project 111 of China.
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