Cycas fushunensis sp. nov. (Cycadaceae) from the Eocene of

Transcription

Cycas fushunensis sp. nov. (Cycadaceae) from the Eocene of
Review of Palaeobotany and Palynology 204 (2014) 43–49
Contents lists available at ScienceDirect
Review of Palaeobotany and Palynology
journal homepage: www.elsevier.com/locate/revpalbo
Research paper
Cycas fushunensis sp. nov. (Cycadaceae) from the Eocene of
northeast China
Kui Su a, Cheng Quan b,⁎, Yu-Sheng (Christopher) Liu c,⁎⁎
a
b
c
MLR Key Laboratory of Saline Lake Resources and Environments, Institute of Mineral Resources, CAGS, Beijing 100037, China
Research Center of Stratigraphy and Paleontology, Jilin University, Changchun, Jilin 130026, China
Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37614, United States
a r t i c l e
i n f o
Article history:
Received 7 December 2013
Received in revised form 24 February 2014
Accepted 25 February 2014
Available online 3 March 2014
Keywords:
Cycas
Cycadaceae
leaflet
epidermal anatomy
fossil and living species
a b s t r a c t
A new cycad species, Cycas fushunensis sp. nov., is described from the Lutetian Jijuntun Formation at Fushun
Coalmine, Liaoning Province, northeast China, based on a well-preserved partial frond containing about 15 leaflets. The fossil is characterized by a single strong vein per leaflet, decurrent leaflet base and haplocheilic stomata,
suggesting that the fossil is attributed to the genus Cycas of Cycadaceae. Epidermal anatomical comparisons between the fossil and 17 selected modern Cycas species further indicate that C. fushunensis sp. nov. closely resembles Cycas panzhihuaensis Zhou et Yang, an endemic cycad to southwest China, due to characters shared, such as
the straight anticlinal walls of both adaxial and abaxial epidermal cells and granular to striate cuticular characters
on the internal surface of guard cell periclinal walls. The occurrence of close-to-modern Cycas from the early
Cenozoic largely casts doubt on a hypothesis of the late Miocene differentiation of modern cycads, suggested
by a recent molecular phylogenetic study.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
The genus Cycas of the Cycadaceae has about 90 living species distributed in the tropical and subtropical lowlands of Southeast Asia,
Madagascar, East Africa, north and northeast Australia, and southwest
Pacific (Hill, 1992; Jones, 1993; Shen et al., 1994; Hill et al., 2004a,
2004b; Stanberg and Stevenson, 2012). In China, there are at least 16 extant species living in seasonal dry regions of south and southwest China
(Guan et al., 1996). Although the genus is not diverse, the state of
its taxonomy is quite confusing and work on its systematics is far
from satisfactory (Jones, 1993; Guan et al., 1996; Whitelock, 2002;
Hill, 2003; Chen and Liu, 2004). New records of living species are still
emerging (e.g., Hill et al., 2004a, 2004b; Singh and Radha, 2008; Agoo
and Madulid, 2012). Fortunately, studies on leaf epidermal morphology
and stomatal structure using light microscopy (LM) (Greguss, 1957;
Pant and Nautiyal, 1963; Greguss, 1965, 1968; Wang and Chen, 1995)
and particularly scanning electron microscopy (SEM) (Wang and
Chen, 1995) have indicated that foliar epidermal features can be fairly
diagnostic in the absence of reproductive cones and seeds. Using principal component analysis under normalized variables, Mickle et al. (2011)
⁎ Correspondence to: C. Quan, Research Center of Paleontology and Stratigraphy, Jilin
University, 938, Xi-minzhu Str., Changchun, 130026, China. Tel.: +86 431 8860 5530;
fax: +86 431 8850 2427.
⁎⁎ Correspondence to: Y.-S. Liu, Department of Biological Sciences, 309 Brown Hall, East
Tennessee State University, Box 70703, Johnson City, TN 37614-1710, USA. Tel.: +1 423
439 6920; fax: +1 423 439 5958.
E-mail addresses: quan@jlu.edu.cn (C. Quan), liuc@etsu.edu (Y.-S.(C.) Liu).
http://dx.doi.org/10.1016/j.revpalbo.2014.02.008
0034-6667/© 2014 Elsevier B.V. All rights reserved.
demonstrated that foliar epidermal features can likely facilitate the separation of five commonly confused living species of Cycas.
Due to their richness and diversity in Mesozoic fossil records cycadophytes have been considered to be an evolutionarily ancient seed plant
group (Taylor et al., 2009). However, a recent study of fossil-calibrated
phylogenies on living cycads indicated that these modern species
evolved from a small number of ancestor species that lived no more
than ~12 Ma (late Miocene) (Nagalingum et al., 2011). This conclusion
may still need further elaboration as numerous pre-Miocene cycadean
records have been documented (e.g. Hill, 1980; Horiuchi and Kimura,
1987; Kvaček, 2002; Erdei et al., 2012), strongly depicting an earlier
differentiation of cycadean evolution. Here we report a new Eocene
leaf species attributed to Cycas from northeast China. The leaf fossil
was briefly reported by Liu et al. (1990) and cuticularly studied by Liu
(1992), but its taxonomical treatment has not been validly published.
In the past decades, new information on the taxonomy of Cycas has become available and it is now possible that the fossil can likely be recognized by its distinctive epidermal characters and better compared with
living species, particularly Cycas panzhihuaensis, a Chinese endemic and
the most similar living Cycas species to this Eocene species.
2. Material and methods
The Fushun Coalmine is located in an east–west trending exposure
of Mesozoic and Cenozoic rocks surrounded by Precambrian terrain
(Wu et al., 2002). The well-exposed strata occurring in the coalmine
are along the slopes of excavated pits. These continental sequences
44
K. Su et al. / Review of Palaeobotany and Palynology 204 (2014) 43–49
85
A
100
115
N
pЄ
B
45
Fushun
45
Fushun
K 1lf
China
35
K 1lf
pЄ
E 2gj
35
E 2x
E 2j
25
E 1lz
25
E 2g
500 km
15
85
E 1l
1 km
100
115
pЄ
1
K 1lf
pЄ
2
3
4
5
6
7
8
9
10
Fig. 1. Map showing the location where the regional stratigraphy in Fushun Coalmine is distributed and the fossil was uncovered. 1. Pre-Cambrian; 2. Lower Cretaceous Longfengkan
Formation; 3. Selandian Laohutai Formation; 4. Thanetian Lizigou Formation; 5. Ypresian Guchengzi Formation; 6. Lutetian Jijuntun Formation; 7. Bartonian Xilutian Formation; 8.
Priabonian Gengjiajie Formation; 9. Fault; 10. Fossil location in the lower part of the Jijuntun Formation.
Plate I. Fossil leaf of Cycas fushunensis sp. nov. from the Lutetian in Fushun, northeastern
China. Holotype PB 16728. Scale bar = 5 cm. One slab specimen, showing the leaf frond
with 15 pinnae attached. Note the apex of leaflet is not preserved and the diverging angles
on both sides of rachis are different, probably due to the preservation.
consist of fluvio-deltaic and tuffaceous sediments that were deposited
in the basin during the early Paleogene (Wu et al., 2002). In ascending
order, the sequence is subdivided into the Laohutai, Lizigou, Guchengzi,
Jijuntun, Xilutain, and Gengjiajie formations (See Fig. 1). This sedimentary sequence across the Selandian (mid Paleocene) to Priabonian (late
Eocene) lacks noticeable unconformities except for the para-conformity
between the first two formations (Zhao et al., 1992). The continuous
Paleogene strata, although in part of the upper sections, represent one
of the best sediments for paleoecological studies in East Asia (Quan
et al., 2011, 2012a, 2012b). In addition to the abundant palynological
records, the ages of these formations have been constrained by data
of either paleomagnetism, isotopes, or insect fossils (Quan et al., 2011).
The plant macrofossils, mainly leaves, are preserved only in the
lower part of the oil shale and black shale Jijuntun Formation. Paleomagnetic dating suggests that the fossiliferous layer of the Formation
is 47.5 ± 1 Ma, viz. the Lutetian (early Middle Eocene) (Quan et al.,
2011). One slab with the compression of a Cycas leaf fossil with several
attached leaflets and its counterpart were found in the oil shale, in
which many other plant taxa, such as Sabalites, Mimosites, Firmiana,
Meliosma, Phellodendron, Quercus, Acer, Rhus and Betula, were uncovered (Liu et al., 1996). An updated list of genera in the leaf flora can be
seen in the appendix of Quan et al. (2011).
The fossil Cycas leaf yielded well preserved cuticles. For a cuticular
analysis, small carbonized fragments on the fossil were directly sampled
from a centrally located leaflet. After being treated in 47% hydrofluoric
acid for two days, the samples were thoroughly washed in distilled
water and then macerated in Schulze solution until the organic material
was oxidized (Kerp, 1990; Pott and McLoughlin, 2009). For comparisons, modern Cycas leaves were obtained from various Chinese herbaria
and the Australian species were requested from the National Herbarium
of New South Wales (Liu, 1992). The modern cuticles were prepared by
treating samples with 20% Cr2O3 (Alvin and Boulter, 1974) for up to
96 h. Cross section of the modern samples follows the standard paraffin
embedding and sectioning (Ruzin, 1999). For SEM observations, the
fossil and modern cuticles were washed in distilled water, mounted
abaxially and adaxially on stubs with double-sided tape and air dried.
The cuticle was sputter coated and examined with JEOL SEM at 20 kV.
The fossil cuticles, although well-preserved, are quite fragmentary.
The terminology for cuticle morphology follows Stockey and Frevel
(1997) and Mickle et al. (2011).
3. Systematics
Family: CYCADACEAE Persoon, 1807
Genus: Cycas L., 1753
Species: Cycas fushunensis Su, Quan et Liu, sp. nov.
Holotype: PB 16728 (Plate I; Plate II, 1–8) and PB 16727 (counterpart).
Plate II. Scanning electron micrographic images of cuticles of Cycas fushunensis sp. nov. Scale bar = 100 μm for images 1 and 5; 10 μm for images 2–4, 6–8. 1–2. Adaxial epidermis. 1. Smooth
external surface, showing the outline of rectangular adaxial epidermal cells. 2. Internal surface, showing slightly granular periclinal walls of epidermal cells. 3–8. Abaxial epidermis.
3. External surface, showing a slightly sunken stoma. 4. External surface, showing an enlarged round base. 5. Internal surface, showing regularly distributed stomata near the central
vein (left of photo). Note the stomata near the central vein parallel the vein course. 6. Internal surface of a haplocheilic stoma, encircled by about nine subsidiary cells. 7. Internal surface,
showing granular striae periclinal walls of two guard cells. 8. External surface, showing another slightly sunken stoma with a short opening slit.
K. Su et al. / Review of Palaeobotany and Palynology 204 (2014) 43–49
45
46
K. Su et al. / Review of Palaeobotany and Palynology 204 (2014) 43–49
Table 1
Comparisons of characteristic epidermis between Cycas fushunensis sp. nov. and seventeen selected modern species of Cycas (based on Liu, 1992; Wang and Chen, 1995; Mickle
et al., 2011).
Taxa
C. fushunensis
C. angulata
C. armstrongii
C. balansae
C. basaltica
C. cairnsiana
C. calcicola
C. circinalis
C. furfuracea
C. guizhouensis
C. media
C. micholitzii
C. panzhihuaensis
C. pectinata
C. revoluta
C. rumphii
C. siamensis
C. szechuanensis
Anticlinal wall
External surface
Subsidiary cells
Adaxial
Abaxial
Adaxial
Abaxial
Number
Straight
Straight
Straight
Undulate
Straight
Straight
Straight
Straight
Straight
Straight
Straight
Undulate
Straight
Undulate
Undulate
Straight
Straight
Undulate
Straight
Straight
Straight
Undulate
Straight
Straight
Straight
Undulate
Straight
Undulate
Straight
Undulate
Straight
Undulate
Straight
Undulate
Straight
Undulate
Smooth
Papillar
Irregular
Smooth
Papillar
Papillar
Irregular
Smooth
Irregular
Irregular
Irregular
Smooth
Smooth
Papillar
Papillar
Smooth
Irregular
Smooth
Smooth
Papillar
Papillar
Papillar
Papillar
Papillar
Papillar
Smooth
Papillar
Papillar
Papillar
Smooth
Smooth
Papillar
Papillar
Papillar
Smooth
Papillar
9
8–10
7–10
5
8–10
9–11
8–9
9–10
8–10
6–9
8–10
6–7
8–11
10–12
14–20
10–11
8–10
6–8
Locality
China
Australia
Australia
Viet Nam
Australia
Australia
Australia
Comoros
Australia
China
Australia
China
China
China
China
China
China
China
Table 2
Habit comparisons between Cycas fushunensis sp. nov. and seventeen selected modern species of Cycas (data compiled from Zhou et al., 1990; Jones, 1993; Stanberg and Stevenson, 2012).
Taxa
Distribution
Habitat
C. fushunensisa
C. angulata
C. armstrongii
C. balansae
C. basaltica
C. cairnsiana
C. calcicola
C. circinalisb
C. furfuracea
C. guizhouensis
C. media
C. micholitzii
C. panzhihuaensis
C. pectinata
C. revoluta
C. rumphii
C. siamensis
C. szechuanesis
NE China
N Australia
N Australia
N Vietnam, SW China
NW Australia
NE Australia
NW Australia
E Africa
NW Australia
SW China
NE Australia
C Vietname, E Laos
SW China
SE Asia
SE China, S Japan
SE Asian islands
SE Asia
SE China
Warm, moist, rainy season in summer, little rain in winter.
On sandy soil; tropical with hot, wet, humid summers and long, dry, mild winters.
Monsoonal with hot, wet, humid summer and long, dry, mild winters.
Tropical with hot, humid summers and warm, moist to dry winters.
Tropical with hot, wet, humid summers and long, dry winters.
Tropical with wet summers and dry winters.
Tropical with wet, humid summers and dry winters.
Hot and humid in summer and mild and frost free in winter
Tropical with wet summers and dry winters.
On poor soil; rainy, moist and cool summers and moist and frost-free winters.
Tropical with hot, wet, humid summers and drier winters.
Tropical with rainy, warm and moist climate.
Subtropical with hot, humid summers and cold, dry with severe frosts winters.
On poor soil; tropical with wet, humid summers and mild, dry winters.
Mild in summer and cold in winters.
Tropical with hot, wet, humid summers and mild, moist to dry winters.
Rainy, tropical with hot, humid summers and mild, dry winters.
Warm, fine rain and little sunshine, hot rainy climate.
a
b
Paleoenvironment and climate reconstructions from WGCPC (1978).
The name of this species should be transferred to Cycas thouarsii R.Br. ex Gaudich. (See Jones, 1993, p. 161.)
Repository: The two fossil specimens and their cuticle samples are all
kept in the Nanjing Institute of Geology and Palaeontology, Chinese
Academy of Sciences.
Type stratum and locality: Lower part of the Jijuntun Formation of Fushun Coalmine, Fushun, Liaoning Province, northeast China (41°50′N,
123°54′E).
Age: Lutetian (early Middle Eocene).
Etymology: The specific epithet fushunensis is given to represent the
type locality where the fossil was uncovered.
Diagnosis: Pinnately compound leaf consisting of alternate leaflets; leaf
rachis with furrows, straight and strong; leaflet linear, entire margined,
and coriaceous; single central vein per leaflet; leaf hypostomatic, stomata haplocheilic, slightly sunken, epidermal cells mainly rectangular, cell
walls straight, internal surface of epidermal cells with paralleling rodlike microstructures.
Description:
The fossil specimen (part and counterpart) consists of a single leaf
portion, which is segmented into several leaflets (Plate I). Totally, 15
leaflets are preserved; however, all are incomplete with their apices
lacking (Plate I). Leaflets are entirely margined with slightly recurved
margins. Leaflets are arranged alternately and appear to have different
diverging angles along the two sides, viz. 40–45° on one side, and 80°
on the other (probably resulting from preservation). Leaflets are linear
and coriaceous. The longest preserved leaflet is about 150 mm in length,
7–8.5 mm in width; the leaflet apex is unknown, and its base is somewhat decurrent (Plate I). One central vein, straight and 1.2 mm wide, occurs per leaflet and is protruding on both sides. Distance between
adjacent leaflets is 9–11 mm. Frond rachis is straight and 5 mm wide.
Eight furrows occur on the abaxial surface of rachis.
The leaflet is hypostomatic. Cuticles are robust.
Plate III. Scanning electron micrographs of two selected modern Cycas epidermis for comparison. Scale bar = 1 μm for images 2, 3, 8; 10 μm for images 1, 4, 6, 7; 100 μm for image 5. 1–4.
Cycas guizhouensis. Fresh leaf samples were requested from Guizhou Agriculture College. 1. Abaxial internal surface, showing a stoma. 2. Abaxial internal surface of a guard cell, showing
coarse granular components on periclinal wall. 3. Adaxial internal surface of an epidermal cell, showing interweaved rods and a few granules on periclinal wall. 4. Abaxial external surface
of a stoma. Note the stoma is only slightly sunken. 5–8. Abaxial epidermis of Cycas panzhihuaensis. Fresh leaf samples were collected in Lushan Botanical Garden of eastern China. 5. Internal
surface, showing four stomata. Note about nine subsidiary cells with each stoma. 6. Internal surface of a guard cell, showing fine granules and striae on periclinal wall. 7. A cross section of a
sunken stoma. 8. Internal surface of an epidermal cell, showing granular components on periclinal wall.
K. Su et al. / Review of Palaeobotany and Palynology 204 (2014) 43–49
47
48
K. Su et al. / Review of Palaeobotany and Palynology 204 (2014) 43–49
Adaxial epidermal cells are generally elongate, rectangular, 32–76 μm
long and 6–30 μm wide (Plate II, 1). These cells are randomly arranged.
Anticlinal walls appear straight (Plate II, 1, 2). SEM observations reveal
that the external surface is smooth (Plate II, 1), whereas the internal
surface appears somewhat smooth or slightly granular (Plate II, 2). Epidermal cells over the central vein are rectangular and regularly arranged,
with their long axes paralleling the vein course (Plate II, 5). Their anticlinal walls are straight and about 2 μm thick. Leaflet marginal epidermal
cells become elongated and narrow, 131 μm in length and only 13 μm
in width. Their anticlinal walls are straight.
Abaxial epidermal cells are mainly rectangular, 35–73 μm long and
18–29 μm wide (Plate II, 5). They are randomly arranged. Anticlinal
walls are straight and about 2.5 μm thick. Their external surface is
smooth, while the internal surface possesses paralleling rod-like microstructures, among which cuticular pits occur (Plate II, 6). Cuticular
flanges appear thick (Plate II, 2). Stomata are haplocheilic and even
distributed between the margin and central vein. Their arrangement is
oriented along the vein course (Plate II, 5, 6). The stomata are more
or less orbiculate to wide elliptic (Plate II, 6, 7), 36–65 μm long and
25–40 μm in wide and slightly sunken (Plate II, 3, 8). The two rectangular kidney-shaped guard cells are heavily cutinized, particularly in the
polar ends, creating thick flanges. Micromorphologically, the internal
surface of the guard cells appear somewhat granular and striated
(Plate II, 7). The 9 encircling subsidiary cells are 20–25 μm long and
8–15 μm wide and overarch the stomatal pore, forming a slightly
sunken stoma (Plate II, 6, 8).
4. Discussion
The present fossil is characterized by the following gross morphological features of leaflet: linear, thick and recurved margin, one vein
per leaflet, and decurrent base (Plate I). These are the diagnostic characters of Cycadaceae (Whitelock, 2002; Linström, 2004; Stanberg and
Stevenson, 2012). Although Stangeria (Stangeriaceae; an endemic to
South Africa) has a single central vein per leaflet, it can be readily distinguished from Cycadaceae since Stangeria also has numerous lateral
veins diverging from the central vein and forming dichotomous
branches (Stanberg and Stevenson, 2012). Furthermore, there are two
leaflet attachment patterns in Cycadales (Stanberg and Stevenson,
2012). The first pattern is decurrent, which occurs in Cycas, Dioon,
Encephalartos, Lepidozamis, Macrozamia, Stangeria and Bowenia, whereas the second type is articulate, which can be seen in Ceratozamia,
Chigua, Microcycas and Zamia (Stevenson, 1990; Whitelock, 2002). The
combination of gross morphological features clearly supports that the
Chinese fossil is strongly related to Cycadaceae and is at best assigned
to the genus Cycas.
4.1. Comparison with Cenozoic species of Cycas
While Cycadales are distinctive on the basis of several characters
unique to the order, such as girdling leaf traces, an inverted-omegashaped pattern of the petiole vascular bundles, coralloid roots, and
primary thickening meristems, definitively assigning fossil leaves to
Cycadales can be difficult (e.g. Harris, 1964; Hill, 1980; Kvaček, 2002,
2004; Hermsen et al., 2007; Pole, 2007; Erdei et al., 2012). In the absence
of reproductive organs, leaf epidermal anatomy, combined with foliar
macromorphology, may provide diagnostic features (Wang and Chen,
1995; Mickle et al., 2011; Erdei et al., 2012). As Cycas fushunensis is
from the Eocene, the comparison therefore is confined to the Cenozoic
records. The reliable records of Cenozoic cycads are relatively scanty,
implied by the dramatic decrease in the geographic range and diversity
of cycads starting in the late Cretaceous and continuing through the
Cenozoic (Horiuchi and Kimura, 1987; Pant, 1987; Kvaček, 2002,
2004; Erdei et al., 2012). They are mainly represented by members
of the Stangeriaceae and Zamiaceae, such as Bowenia (Hill, 1978),
Ceratozamia (Kvaček, 2002, 2004), Dioonopsis (Horiuchi and Kimura,
1987; Erdei et al., 2012), Eostangeria (Kvaček and Manchester, 1999)
and Macrozamia (Carpenter, 1991). However, the fossil records of
Cycadaceae are extremely rare.
Fossil Cycas leaves from the Cenozoic have been reported previously,
e.g. Cycas fujiiana Yokoyama from the Palaeogene of southern Japan
(Yokoyama, 1911) and Cycas cretacea Krassilov from the Santonian,
Late Cretaceous of Sakhalin (Krassilov, 1978, 1979). Cycas fujiiana is an
impression fossil without any anatomical structure preserved. Pant
(1987) considered that it is close to Cycas revoluta but did not give
any further evidence. After checking the type specimen, we tend to
believe that it is different from Cycas fushunensis that the leaflets
of C. fujiiana have no decurrent base and its leaflet is much smaller
than that of C. fushunensis. On the other hand, C. cretacea is preserved
with cuticles showing a great similarity to C. revoluta (Krassilov, 1978,
1979) rather than to C. fushunensis. In addition, the Sakhalin fossil has
much smaller leaflets than the Chinese fossil.
In conclusion, the Chinese fossil can undoubtedly be separated from
any other Cenozoic cycads due to its pinnately compound leaf, leaflet
with a single central vein, and the presence of sunken haplocheilic stomata (e.g., Steward and Rothwell, 1993; Taylor et al., 2009).
4.2. Cuticle comparisons with living Cycas
The leaf cuticle study of fossil and extant Cycadales has long been conducted since 1856 (Bornemann, 1856) and ever since many others have
continuously expanded to include more cycad species and mainly focused
on their taxonomic problems, most of which were examined under LM
(Strasburger, 1866–1867; Mahlert, 1885; Thomas and Bancroft, 1913;
Greguss, 1957; Bobrov, 1962; Pant and Nautiyal, 1963; Greguss, 1965,
1968; Stevenson, 1981; Wang and Chen, 1995). In the past several decades, SEM observations on gymnospermous foliage cuticles have proven
powerful in taxonomic research (e.g. Stockey and Frevel, 1997; Mickle
et al., 2011). In the present study, the cuticle comparisons are mostly
based on SEM investigations. Taxonomically sound cuticle characters of
the Chinese fossil and selected 17 living species are compared (Table 1).
Among the living species of Cycas studied here, 4 southeast Asian
species, i.e. Cycas micholitzii, Cycas szechuanesis, Cycas balansae and
Cycas pectinata, have undulate anticlinal walls on both adaxial and abaxial epidermal cells (Table 1). Only one species (Cycas revoluta) has sinuous walls restricted to the adaxial epidermis (Table 1), while Cycas
circinalis and Cycas guizhouensis have undulate walls on the abaxial epidermis only (Table 1). It is interesting that all the species from Australia
surveyed here have straight anticlinal wall (Table 1).
The adaxial external surface of epidermal cells in Cycas displays
three types of wall ornamentation, viz. smooth, papillar and irregular
(Table 1). All Australian species examined and several Asian species
have irregularly cuticular platelets or papillae on their adaxial external
surface, whereas the remaining species including Cycas fushunensis
have a smooth adaxial external surface (Table 1; Plate II, 1). In the
case of the abaxial external surface of the epidermal cells, most of the
Australian species have conspicuous papillae (Table 1), which are, in
combination with deeply sunken stomata corresponding to their dry
habitat (Table 2; Liu, 1992). Only a few of other species are abaxially
more or less smooth, such as Cycas panzhihuaensis, Cycas siamensis,
Cycas circinalis, Cycas micholitzii and the Chinese fossil C. fushunensis
(Table 1; Plate II, 3, 8).
The internal cuticle surface of the guard cells in most species is
generally granular, only a few species including Cycas fushunensis
and Cycas panzhihuaensis have a combination of granules and striae
(Plate II, 7; Plate III, 6). Because of this comparative similarity in the
guard cells, plus both species sharing the straight anticlinal walls and
smooth external surface of their adaxial and abaxial epidermal cells
and about 9 subsidiary cells per stoma (Table 1), C. fushunensis is therefore believed to be closest to C. panzhihuanensis.
In summary, the Chinese fossil is morphologically close to Cycas of
the Cycadaceae, and has epidermal anatomical characters comparable
K. Su et al. / Review of Palaeobotany and Palynology 204 (2014) 43–49
with those of the living Cycas examined here. In particular, it closely resembles Cycas panzhihuaensis, an endemic cycad in southwest China.
The fossil provides an early Cenozoic record of Cycas and consequently
a proposed late Miocene differentiation may be reconsidered by a recent
fossil-calibrated molecular phylogenetic analysis (Nagalingum et al.,
2011; Renner, 2011). From a paleobotanical point of view, the limitations of molecular systematics were well addressed by Axsmith et al.
(1998). As Mao et al. (2012) later commented, molecular-clock studies
of gymnosperms consistently have inferred young ages for the crown
groups of living genera, probably due to the extinction of entire clades.
This present study further demonstrates the crucial importance of fossil
records in building the “Tree of Life.”
Acknowledgments
Thanks are due to the keepers of various herbaria and botanical
gardens in China for sending living cycad leaf samples. Dr. Christian
Pott and an anonymous reviewer are thanked for their constructive
comments. The research is supported in part by NSFC 41172008 and
41372002 to C.Q. and ETSU RDC grant to Y.S.L.
References
Agoo, E.M.G., Madulid, D.A., 2012. Cycas sancti-lasallei (Cycadaceae), a new species from
the Philippines. Blumea 57, 131–133.
Alvin, K.L., Boulter, M.C., 1974. A controlled method of comparative study for taxodiaceous
leaf cuticles. Bot. J. Linn. Soc. 69, 277–286.
Axsmith, B.J., Taylor, E.L., Taylor, T.N., 1998. The limitations of molecular systematics:
a palaeobotanical perspective. Taxon 47 (1), 105–108.
Bobrov, A.E., 1962. Comparative investigation of the epidermis and the stomata of the
leaves of Cycadaceae. Bot. J. USSR 47 (6), 808–820.
Bornemann, J.G., 1856. Über organische Reste der Lettenkohlengruppe Thüringens.
Engelmann, Leipzig.
Carpenter, R.J., 1991. Macrozamia from the Early Tertiary of Tasmania and a study of the
cuticles of extant species. Aust. Syst. Bot. 4, 433–444.
Chen, C.J., Liu, N., 2004. New discoveries of cycads and advancement of conservation of
cycads in China. Bot. Rev. 70 (1), 93–100.
Erdei, B., Manchester, S.R., Kvaček, Z., 2012. Dioonopsis Horiuchi et Kimura leaves from the
Eocene of Western North America: a cycad shared with the Paleogene of Japan.
Intern. J. Plant Sci. 173 (1), 81–95.
Greguss, P., 1957. The leaf-epidermis of the Cycadales. Acta Biol. (Szeged) 3, 151–164.
Greguss, P., 1965. The relationships of Cycadales on the basis of their xylotomy, branching
and leaf epidermis. Palaeobotanist 14, 94–101.
Greguss, P., 1968. Xylotomy of the Living Cycads, with a Description of Their Leaves and
Epidermis. Adaemiai Kiado, Budapest.
Guan, Z., Zhou, L., Hsu, K., 1996. Classification and distribution of cycads. In: Guan, Z.
(Ed.), Cycads of China. Sichuan Science and Technology Press, Chengdu, pp. 4–26
(in Chinese).
Harris, T.M., 1964. The Yorkshire Jurassic Flora. 2. Caytoniales, Cycadales and
PteridospermsBritish Museum (Natural History), London.
Hermsen, E., Taylor, T.N., Taylor, E.L., Stevenson, D.W., 2007. Cycads from the Triassic of
Antarctic: permineralized cycad leaves. Int. J. Plant Sci. 168 (7), 1099–1112.
Hill, R.S., 1978. Two new species of Bowenia Hook. Ex Hook. F. from the Eocene of Eastern
Australia. Aust. J. Bot. 26, 837–846.
Hill, R.S., 1980. Three new Eocene cycads from eastern Australia. Aust. J. Bot. 28, 105–122.
Hill, K.D., 1992. A preliminary account of Cycas (Cycadaceae) in Queensland. Telopea 5 (1),
177–206.
Hill, K.D., 2003. The families and genera of cycads: a molecular phylogenetic analysis of
Cycadophyta based on nuclear and plastid DNA sequence. Int. J. Plant Sci. 164,
933–948.
Hill, K.D., Nguyen, H.T., Loc, P.K., 2004a. The genus Cycas (Cycadaceae) in Vietnam. Bot.
Rev. 70, 134–193.
Hill, K.D., Stevenson, D.W., Osborne, R., 2004b. The world list of cycads. In: Walters, T. (Ed.),
Cycad Classification: Concepts and Recommendations. CABI Publishing, Wallingford,
Oxon.
Horiuchi, J., Kimura, T., 1987. Dioonopsis nipponica gen. et sp. nov., a new cycad from the
Palaeogene of Japan. Rev. Palaeobot. Palynol. 51, 213–225.
Jones, D.L., 1993. Cycads of the World — Ancient Plants in Today's Landscape. Smithsonian
Institution Press, Washington D.C.
Kerp, H., 1990. The study of fossil gymnosperms by means of cuticular analysis. Palaios 5,
548–569.
Krassilov, V.A., 1978. Late Cretaceous gymnosperms from Sakhalin and the terminal
Cretaceous event. Palaeontology 21 (4), 893–905.
Krassilov, V.A., 1979. The Cretaceous flora of Sakhalin. Project N j58 (Mid-Cretaceous
Events) of the International Geological Correlation ProgrammePublishing House
“Nauka”, Moscow.
49
Kvaček, Z., 2002. A new Tertiary Ceratozamia (Zamiaceae, Cycadopsida) from the
European Oligocene. Flora Morphol. Distrib. Funct. Ecol. Plants 197 (4), 303–316.
Kvaček, Z., 2004. A noteworthy cycad, Ceratozamia hofmannii Ettingshausen 1887, from
the Lower Miocene of Austria re-examined. Neues Jb. Geol. Paläontol. Monat. 2004,
111–118.
Kvaček, Z., Manchester, S.R., 1999. Eostangeria Barthel (extinct Cycadales) from the
Palaeogene of western North America and Europe. Int. J. Plant Sci. 160, 621–629.
Linström, A., 2004. Morphological characters useful in determining species boundaries in
Cycas (Cycadaceae). In: Walters, T., Osborne, R. (Eds.), Cycad Classification: Concepts
and Recommendations. CABI Publishing, Wallingford, Oxfordshire, UK, pp. 45–55.
Liu, Y.S., 1992. First discovery of Cycas fossil pinnae in China with comments on the
phylogeny and historical phytogeography of Cycas. (Ph.D. Thesis) Nanjing Institute
of Geology & Palaeontology, Chinese Academy of Sciences, Nanjing, China (in Chinese
with English summary).
Liu, Y.S., Zhou, Z.Y., Li, H.M., 1990. First discovery of Cycas megafossil in China. Chin. Sci.
Bull. 22, 1758–1759 (in Chinese).
Liu, Y.S., Guo, S.X., Ferguson, D.K., 1996. A catalogue of Cenozoic megafossil plants in
China. Palaeontogr. Abt. B Palaeophytologie 238, 141–179.
Mahlert, A., 1885. Beiträge zur Kenntnis der Anatomie der Laubblätter der Coniferen, mit
besonderer Berücksichtigung des Spaltöffungs-Apparates. Bot. Centralbl. 24, 54.
Mao, K., Milne, R.I., Zhang, L., Peng, Y., Liui, J., Thomas, P., Mill, R.R., Renner, S.S., 2012.
Distribution of living Cupressaceae reflects the breakup of Pangea. Proc. Natl. Acad.
Sci. U. S. A. 109 (20), 7793–7798.
Mickle, J.E., Rosaria Barone Lumaga, M., Moretti, A., De Luca, P., 2011. Scanning electron
microscopy studies of cuticle micromorphology in Cycas L. (Cycadaceae). Plant
Biosyst. 145 (1), 191–201.
Nagalingum, N.S., Marshall, C.R., Quental, T.B., Rai, H.S., Little, D.P., Mathews, S., 2011.
Recent synchronous radiation of a living fossil. Science 334, 796–799.
Pant, D.D., 1987. The fossil history and phylogeny of the Cycadales. Geophytology 17 (2),
125–162.
Pant, D.D., Nautiyal, D.D., 1963. Cuticle and epidermis of recent of Cycadales: leaves,
sporangia and seeds. Senckenberg. Biol. 44, 257–347.
Pole, M.S., 2007. Conifer and cycad distribution in the Miocene of southern New Zealand.
Aust. J. Bot. 55, 143–164.
Pott, C., McLoughlin, S., 2009. Bennettitalean foliage in the Rhaetian–Rajocian (latest
Triassic–Middle Jurassic) floras of Scania, southern Sweden. Rev. Palaeobot. Palynol.
158, 117–166.
Quan, C., Liu, Y.S., Utescher, T., 2011. Paleogene evolution of precipitation in northeastern
China supporting the middle Eocene intensification of the East Asian monsoon.
Palaios 26, 743–753.
Quan, C., Liu, Y.S., Utescher, T., 2012a. Paleogene temperature gradient, seasonal variation
and climate evolution of northeast China. Palaeogeogr. Palaeoclimatol. Palaeoecol.
313–314, 150–161.
Quan, C., Liu, Y.S., Utescher, T., 2012b. Eocene monsoon prevalence over China: a paleobotanical perspective. Palaeogeogr. Palaeoclimatol. Palaeoecol. 365–366, 302–311.
Renner, S.S., 2011. Living fossil younger than thought. Science 334, 766–767.
Ruzin, S.E., 1999. Plant Microtechnique and Microscopy. Oxford University Press,
New York.
Shen, C.-F., Hill, K.D., Tsou, C.H., Chen, C.J., 1994. Cycas taitungensis C.F. Shen, K.D. Hill, C.H.
Tsou & C.J. Chen, sp. nov. (Cycadaceae), a new name for the widely known cycad
species endemic in Taiwan. Bot. Bull. Acad. Sin. 35, 133–140.
Singh, R., Radha, P., 2008. A new species of Cycas (Cycadaceae) from Karnataka, India. Bot.
J. Linn. Soc. 158, 430–435.
Stanberg, L., Stevenson, D., 2012. The Cycad pages. Available http://plantnet.rbgsyd.nsw.
gov.au/Plantnet/cycad/index.html (accessed December 4, 2013).
Stevenson, D.W., 1981. Observations on ptyxis, phenology, and trichomes in the
Cycadales and their systematic implications. Am. J. Bot. 68, 1104–1114.
Stevenson, D.W., 1990. Morphology and systematics of the Cycadales. Mem. N. Y. Bot.
Gard. 57, 8–55.
Steward, W.H., Rothwell, G.W., 1993. Paleobotany and the Evolution of Plants, 2nd edition.
Cambridge University Press, Cambridge.
Stockey, R.A., Frevel, B.J., 1997. Cuticle micromorphology of Prumnopitys Phillipi
(Podocarpaceae). Intern. J. Plant Sci. 158, 198–221.
Strasburger, E., 1866–1867. Ein Beitrag zur Entwicklungsgeschichte der Spaltöffnung.
Jahrb. Wiss. Bot. 5, 297–342.
Taylor, T.N., Taylor, E.L., Krings, M., 2009. Paleobotany—The Biology and Evolution of Fossil
Plants. Academic Press, Burlington, MA, USA.
Thomas, H.H., Bancroft, N., 1913. On the cuticle of some recent and fossil cycadean fronds.
Transactions of the Linnean Society of London, 2nd series. Botany 48, 155–204.
Wang, Y.Z., Chen, C.J., 1995. Leaflet epidermal characters of the Cycas in China and their
taxonomic significance. Chin. Bull. Bot. 12 (Suppl. 1), 47–51.
WGCPC (Writing Group for Cenozoic Plants of China), 1978. Cenozic Plants from China,
Fossil Plants of China, III. Sci. Press, Beijing.
Whitelock, L.M., 2002. The Cycads. Timber Press, Portland, Oregon, USA.
Wu, C., Wang, X., Liu, G., Li, S., Mao, X., Li, X., 2002. Study on dynamics of tectonic evolution in the Fushun Basin, Northeast China. Sci. China Ser. D Earth Sci. 45, 311–324.
Yokoyama, M., 1911. Some Tertiary fossils from the Miike coal-field. J. Coll. Sci. Imp. Univ.
Tokyo 27 (20), 1–16.
Zhao, C., Wei, D., Liu, H., An, J., Wang, J., 1992. A magnetostratigraphic study of lower
Tertiary in the northeast oil–gas-bearing region in China. Acta Pet. Sin. 13 (2),
226–231.
Zhou, L., Yang, S.Y., Zhou, Z., 1990. Investigation of the natural community of Cycas
panzhihuaensis L. Zhou & S.Y. Yang. Mem. N. Y. Bot. Gard. 57, 148–151.