全 文 ：Leaf Epidermal Feature in Clematis (Ranunculaceae)with Reference
to Its Systematic Significance
SHI Jing_Hua , LI Liang_Qian＊
(Laboratory of Systematic and Evolutionary Botany , Institute of Botany , The Chinese Academy of Sciences , Beijing 100093, China)
Abstract: For finding valuable systematic characters , leaf epidermis of 77 taxa , representing 12 sections of
the genus Clematis and three related genera in the Ranunculaceae , were examined mainly by means of light
microscopy (LM), and partially by scanning electron microscopy (SEM).It was shown that the leaf epidermal
cells were usually irregular or polygonal in shape.The patterns of anticlinal walls were straight , arched or un-
dulate.The stomatal apparatus is anomocytic and exists in abaxial epidermis of all species , and in the adaxial
epidermis of some species.Under SEM observation , the leaf epidermis was often striated , seldom nearly
smooth , and often with flakes attached.Evidence from leaf epidermis serves as a criterion for distinguishing the
subsections in sect.Meclatis (Spach)Tamura and in sect.Fruticella Tamura.The results also support that
there are several separate evolutionary processes in the genus Clematis.
Key words: Ranunculaceae;Clematis;leaf epidermis;stomatal apparatus
The genus Clematis belongs to the large and diverse
buttercup family , Ranunculaceae.Botanists generally
considered the family belonging to one of the most primi-
tive groups of flowering plants.Various authors have at-
tempted a classification in the past but could never reach
a consensus (Kuntze , 1885;Tamura , 1956;1987;
1995;Keener , 1975;1982;Wang , 1980;1998;John-
son , 1997;Fu and Hong , 2001;Wu and Raven ,
2001).Any of the classifications is fraught with difficul-
ties for lack of good and consistent characters.Most of the
characters often appear to be incredibly variable(Wu and
Raven , 2001).The classification presented in this study
is a revision of Wang s description (Wu and Raven ,
2001).
Because of the difficulties in the research on Clema-
tis classification , more evidence is needed to establish a
more perfect systematic construction.Leaf epidermis char-
acteristics are of great taxonomical importance.However ,
in the genus Clematis , leaves of only few taxa have been
examined (Décamps , 1974;Grey_Wilson , 2000).
Therefore , more detailed work , describing the character-
istics of leaf epidermis of Clematis , is needed.The pur-
pose of this study was to find the significant characters of
leaf epidermis , and to provide materials for further re-
search work on the relationship within this genus.
1 Materials and Methods
Fully expanded leaves of 77 taxa (72 species and
five varieties), representing 12 sections of Clematis and
three related genera in the Ranunculaceae (four species of
Anemone , three species of Pulsatilla and two species of
Naravelia)were harvested from the specimens of several
herbaria(Table 1), except the leaves of Clematis patens
Morr.et Decne which were harvested from living plants
growing in the greenhouse of the Institute of Botany , The
Chinese Academy of Sciences.
The leaves for light microscopy (LM)study were
boiled in water before macerated in 20%NaClO solution.
Pieces of leaf epidermis were stained in a solution of 1%
safranin(in 50%alcohol)before being mounted in gum.
To check the constancy of epidermal structure , two or
more leaves were collected for each species , and at least
three slides were made from different parts of a single
leaf.The stomatal index was calculated using the formula
S/(E +S)×100 , where S denotes the number of stom-
ata per unit area and E the number of epidermal cells of
the same area.Materials for scanning electron microscopy(SEM)observation were directly mounted on stubs with-
out any treatment.After gold sputtering , the specimens
were examined and photographed under a Hitachi S_800.
The data of the long axle of stomatawere analyzed by
statistical method t test.The formulae used were given as
follows:
t=(x1-x2)/(Se2/ n1+Se2/n2)1/2
Se2={S12(n1-1)+S22(n2-1)}/{(n1-1)+(n2-1)}
where n is amount of datum , s is standard deviation and
x is mean.
The terminology followed that of Wilkinson (1979),
and the Wang s classification was adopted (Wu and
Raven , 2001).
2 Results
2.1 Characteristics of leaf epidermis under LM
Hairs were present in most species and usually
denser in the abaxial side.Stomata appeared on the
Received:2002-04-25 Accepted:2002-07-19
Supported by the National Natural Science Foundation of China(30070059).
＊Author for correspondence.E_mail:
植 物 学 报
Acta Botanica Sinica 2003 , 45(3):257-268 http://www.chineseplantscience.com
Table 1 Materials Examined
Taxon Collector Location Specimen No. Herbarium
Anemone davidii Franch. Z.C.ZHANG Unknown 402075 PE
A.flaccida Fr.Schmidt X.L.JIANG Pingwu , Sichuan 10839 PE
A.rivularis Buch._Ham.ex DC. X.LI Sichuan 70622 PE
A.demissa Hook.f.et Thoms. Unknown Hongyuan , Sichuan 9089 PE
Pulsatilla chinensis(Bunge)Regel S.Y.BAO Zhiqu , Shanxi 00049 PE
P.campanella Fisch.ex Kryl. Exped.Xizang Yecheng , Xinjiang 870998 PE
P.cernua(Thunb.)Bercht.et Presl. Y.C.ZHU Fenghuangshan , Liaoning 239 PE
Naravelia pilurifera Hance X.X.LIU Hainan 27669 PE
N.laurifolia Wall. Unknown Indonesia 8888 PE
Clematis potaninii Maxim. X.LI Zhegushan , Sichuan 74387 PE
C.montana Buch._Ham.ex DC. G.H.YANG Emeishan , Sichuan 57685 PE
C.chrysocoma Franch. P.Y.MAO Yunnan 61361 PE
C.fasciculif lora Franch. Exped.Chuanxi Sichuan 1711 PE
C.apiifolia DC. Z.Z.DING Suzhou , Jiangsu 0941 PE
C.apiifolia var.argentilucida Rehd.et Wils. Z.S.REN Chengbu , Hunan 49 PE
C.gratopsisW.T.Wang G.F.LI Nanchuan , Sichuan 64958 PE
C.grandidentata (Rehd.et Wils)W.T.WANG Second Exped.
Huanghe
Shanyang , Shanxi 1479 PE
C.chingii W.T.Wang Z.Y.CAO Ceheng , Guizhou 00615 PE
C.peterae var.trichocarpa W.T.WANG Z.Y.ZHANG Wenxian , Gansu 14413 PE
C.brevicaudata DC. W.L.CHEN Maerkang , Sichuan 7609 PE
C.parviloba Gardn.et Champ. J.S.XIN Suangjiang , Yunnan 1203 PE
C.puberula var.subsericea (Rehd.et Wils)C.T.TING Unknown Gongshan, Yunnan 7067 PE
C.crassifolia Benth. Unknown Pingwu , Sichuan 10694 PE
C.meyeniana Walp. M.Z.LI Xuefengshan , Hunan 3008 PE
C.finetiana Lévl.et Vant. Unknown Changhua , Zhejiang 30636 PE
C.chinensis Osbeck Unknown Sichuan 07526 PE
C.terniflora DC. Unknown Hangzhou , Zhejiang 0983 PE
C.terniflora var.mandshurica(Rapr.)Ohwi Second group of
Exped.Yanbian
Ji lin 269 PE
C.kirilowii Maxim. Unknown Langyashan , Hebei 3287 PE
C.obscura Maxim. K.J.GUAN Shanxi 799 PE
C.dilatata Pei Unknown Longquan , Zhejiang 2710 PE
C.uncinata Champ.ex Benth. W.C.WANG Nanchuan , Chongqing 4519 PE
C.armandii Franch. G.F.LI Sichuan 60038 PE
C.delavayi Franch. Unknown Quancheng , Sichuan 2095 PE
C.hexapetala Pall. Unknown Weixian , Hebei 74101 PE
C.fruticosa Turcz. J.W.WANG Wutaishan , Shanxi 128 PE
C.tomentella(Maxim.)W.T.Wang et L.Q.Li P.Licent Yulin , Shanxi 7087 PE
C.brachiata Thunb. A.Nyanza South Africa 2560 US
C.hirsuta Guill.Perr.et Rich. Buchanan Nyasaland , Africa 1022 US
C.tangutica(Maxim.)Korsh. Z.R.WANG Xiahe , Gansu 10860 PE
C.akebioides(Maxim.)Veitch A.LI Dajin , Sichuan 78220 PE
C.glauca Willd. Y.Q.HE Lanzhou , Gansu 5759 PE
C.intricata Bunge Exped.Huanghe Jingbian , Shanxi 8680 PE
C.orientalis L. Exped.Xizhixinjiang Xinjiang 2667 PE
C.smilacifolia Wall. Z.Y.CAO Ceheng Guizhou 1253 PE
C.fulvicoma Rehd.et Wils. Unknown Yunnan 12530 PE
C.crassipes var.pubipesW.T.Wang Y.L.ZHANG Ledong Hainan 337 PE
C.tashiroi Maxim. Furuse Japan 4378 PE
C.pinnata Maxim. S.Y.HE Baihuashan , Beijing 75637 PE
C.heracleifolia DC. Unknown Hebei 2670 PE
C.courtoisii Hand._Mazz. Unknown Jinzhai , Anhui 0228 PE
C.florida Thunb. Exped.Guangxi Lingui , Guangxi 3954 PE
C.cadmia Buch._Ham.ex Wall. M.Z.ZHANG Anhui 14410 PE
258 植物学报 Acta Botanica Sinica Vol.45 No.3 2003
Table 1 (To be continued)
C.huchouensis Tamura Unknown Liuan , Anhui 2371 PE
C.patens Morr.et Decne. L.XIE Beijing XLZ00215 PE
C.henryi Oliv. S.B.LAN Dongchuan, Yunnan 609 PE
C.urophylla Franch. Exped.Beijing Hunan 4502 PE
C.leschenaultiana DC. Unknown Xiaowutai shan , Hebei 5677 PE
C.buchananiana DC. K.M.FANG Unknown 12912 PE
C.repens Finet et Gagnep. Unknown Emeishang , Sichuan 137 PE
C.dasyandra Maxim. Unknown Pingwu , Sichuan 10694 PE
C.rehderiana Craib X.LI Dajin , Sichuan 75591 PE
C.connata DC. J.W.ZHANG Xizang 0408 PE
C.lasiandra Maxim. K.J.GUAN Baoxing , Sichuan 3009 PE
C.ranunculoides Franch. Unknown Lijiang , Yunnan 22656 PE
C.fusca Turcz. L.ZHANG Yilan , Heilongjiang 1907 PE
C.sibirica Mill. Exped.Xizang Yecheng , Xinjiang 870946 PE
C.macropetala Ledeb. K.J.GUAN Lingkoongshan, Shanxi 00318 PE
C.tosaensis Makino Furuse Japan 27217 PE
C.aristata var.occidentalis Benth. R.Helms Western Australia 24316 US
C.acapulcensis Hook et Arn A.Smith Costarica A656 GH
C.dioica L. E.L.Ekman Stockholm 13943 US
C.gentianoides DC. Melville Tasmania 2519 US
C.glycinoides DC. M.Evans Australia 2659 GH
C.ligusticifolia Nutt.ex Torr.et Gray Anderson USA 7 GH
C.pickeringii A.Gray Saunders New Caledonia 15 US
C.lasiantha Nutt. L.Ahart California , USA 5946 MO
GH , Gray Herbarium of Harvard University;MO , Herbarium of Missouri Botanical Garden;PE , Herbarium of Institute of Botany , The Chinese Academy of Sci-
ences;US , the United States Nat ional Herbarium.
abaxial epidermis of all species , but were absent on the
adaxial side of most species.Of all the materials ob-
served , only a few species exhibited stomata on both sides
were found:Anemone rivularis Buch._Ham.ex DC.(Fig.7), A.demissa Hook.f.et Thoms., Pulsatilla
chinensis (Bunge)Regel (Fig.6), P .campanella
Fisch.ex Kryl., P.cernua (Thunb.)Bercht.et
Presl., Clematis fruticosa Turcz.(Fig.23), C.to-
mentella(Maxim.)W.T.Wang et L.Q.Li , C.cad-
mia Buch._Ham.ex Wall.(Fig.15), C.tangutica(Maxim.)Korsh., C.intricata Bunge.(Fig.8), C.
glauca Willd., C.akebioides (Maxim.)Hort.ex
Veitch (Fig.22), C.orientalis L., C.ligusticifolia
Nutt.ex Torr.et Gray (Figs.20 , 40)and C.gen-
tianoides DC.(Figs.14 , 25).The form of epidermal
cells is polygonal or irregular , with straight to arched(Figs.1-8 , 22 , 23)or undulate (Figs.9-21 , 24-
45)anticlinal walls.The shapes of epidermal cells of the
same species are similar on the adaxial and abaxial sides
in most species and the undulation of anticlinal walls are
usually heavier on the abaxial side.Few species have very
different epidermal cells between the adaxial and abaxial
side, such as C.apiifolia DC.(Fig.2), C.chingii
W.T.Wang (Fig.3), C.brevicaudata DC.(Fig.
26), C.parviloba Gardn.et Champ.and C.crassifolia
Benth.The stomatal apparatus are all anomocytic.The
stomatal index measured on 36 species ranges between
7.0 and 13.3 and between 14.1 and 37.8 respectively
for the adaxial and abaxial sides(Table 2).
2.2 Statistical analysis of the stomata size
We analyzed the datum of the long axle of stomata
with statistical method t text.(Tables 3 , 4).
The results show differences on the size of stomata
among the three genera Anemone , Pulsatilla and Clema-
tis , and reveal differences of the size of stomata between
sect.Cheiropsis and other sections.
2.3 Characteristics of leaf epidermis under SEM
The outlines of the pairs of guard cells of all the ma-
terials investigated are suborbiculate to elliptical.The
rims are almost at the same level with or slightly lower
than the epidermis.The wax ornamentation of the cuticle
is often striated , smooth , or slightly flaky (Table 3).
3 Discussion
3.1 Characteristics of leaf epidermis
Décamps (1974)noticed that C.integrifolia L.
had anomocytic stomatal apparatus.Yang and Huang(1992)reported some characteristics of leaf epidermis of
sect.Viorna.Their results are similar to ours in respect
to the shape of the epidermal cells , the pattern of anticli-
nal wall , the shape of stomata and the ornamentation of
the leaf epidermis.These characters show no much differ-
ence among different species , and are of no significance
in systemic research.
3.2 Size of stomata
Results of our study indicate that in the trib.
Anemoneae , stomata are large in Anemone , small in
SHI Jing_Hua et al:Leaf Epidermal Feature in Clematis(Ranunculaceae)with Reference to Its Systematic Significance 259
Table 2 The characters of leaf epidermis under LM
Genera Sect ions Taxa
Adaxial epidermis
Shape
of cells
Pattern of
anticlinal
walls
Size of
stomata
(μm2)
Stomatal
index
Abaxial epidermis
Shape
of cells
Pattern of
anticlinal
walls
Size of
stomata
(μm2)
Stomatal
index
Anemone L.
Anemone davidii Franch. Irr WU Irr HU 42.2×32.2 29.6
A.flaccida Fr.Schmidt Irr WU Irr HU 45.3×36.2 23.8
A.rivularis Buch._Ham.ex DC. Pol Str_arc 34.2×23.5 15.4 Pol Str_arc 35.9×26.3 29.0
A.demissa Hook.f.et
Thoms.
Irr WU 46.2×34.2 7.2 Irr Undulate 48.8×39.0 25.0
Pulsatilla
Adans.
Pulsatil la chinensis
(Bunge)Regel
Pol Str_arc 33.8×22.8 7.6 Irr WU 34.6×32.4 26.3
P.campanella Fisch.ex Kryl. Irr WU 35.5×25.2 14.6 Irr WU 36.2×25.9 19.8
P.cernua(Thunb.)
Bercht.et Presl.
Pol Str_arc Irr WU
Naravelia
DC.
Naravelia pilurifera Hance Irr Undulate Irr Undulate
N.laurifolia Wall. Irr WU Irr WU
Clematis L.
Cheiropsis
DC.
Clematis potaninii Maxim. Irr WU Irr WU 32.4×24.0
C.montana Buch._
Ham.ex DC.
Irr WU Irr Undulate 35.2×21.0 21.9
C.chrysocoma Franch. Irr WU Irr WU 32.2×25.6
C.fasciculiflora Franch. Irr WU Irr HU 36.4×28.0 24.5
Clematis
C.apiifolia DC. Pol Str_arc Irr Undulate 27.6×21.6
C.api ifolia var.argen-
t ilucida Rehd.et Wils.
Pol Str_arc Irr Undulate 23.8×21.1 27.2
C. gratopsis W. T.
Wang
Irr WU Irr WU
C.grandidentata(Rehd.
et Wils)W.T.Wang
Irr WU Irr WU
29.4×21.2
C.chingii W.T.Wang Pol Str_arc Irr WU 23.8×18.2 37.8
C. peterae var. tri-
chocarpa W.T.Wang
Irr WU Irr Sin 26.5×19.2 23.6
C.brevicaudata DC. Pol Str_arc Irr WU 30.2×21.8 14.1
C.parviloba Gardn.et
Champ.
Pol Str_arc Irr WU 25.2×18.7 23.6
C. puberula var. sub-
sericea (Rehd.et Wils)
C.T.Ting
Irr WU Irr Undulate 24.2×18.2 20.8
C.crassifolia Benth. Irr WU Irr WU 26.8×21.6
C.meyeniana Walp. Irr Undulate Irr Undulate 24.0×23.2
C. finetiana Lévl. et
Vant.
Irr Undulate Irr Undulate 29.6×27.6 30.2
C.chinensis Osbeck Irr HU Irr HU
C.ternif lora DC. Irr Undulate Irr HU 25.1×19.2 24.3
C.ternif lora var.mand-
shurica (Rapr.)Ohwi
Irr Undulate Irr HU 28.4×21.2 16.0
C.kiri lowii Maxim. Irr Undulate Irr HU 21.7×17.3 30.7
C.obscura Maxim. Irr WU Irr Undulate 27.5×22.3 29.5
C.di latata Pei Irr Undulate Irr WU 26.2×24.6
C.uncinata Champ.ex
Benth.
Irr Undulate Irr WU 24.6×22.2 17.9
C.armandii Franch. Irr WU Irr Undulate 30.7×22.7 27.5
Fruticella
Tamura
C.delavayi Franch. Irr Undulate Irr Undulate 27.0×18.8
C.hexapetala Pall. Irr WU Irr WU 28.9×20.8 26.1
C.fruticosa Turcz. Pol Str_arc 27.8×23.8 13.3 Pol Str_arc 28.4×24.0 37.8
C.tomentella (Maxim.)
W.T.Wang et L.Q.Li
Pol Str_arc 26.4×20.6 Pol Str_arc 26.0×19.4
260 植物学报 Acta Botanica Sinica Vol.45 No.3 2003
Table 2 (continued)
Genera Sect ions Taxa
Adaxial epidermis
Shape
of cells
Pattern of
anticlinal
walls
Size of
stomata
(μm2)
Stomatal
index
Abaxial epidermis
Shape
of cells
Pattern of
anticlinal
walls
Size of
stomata
(μm2)
Stomatal
index
Clematis L.
Meclat is
(Spach)
Tamura
C.hirsuta Guill.Perr.
et Rich.
Pol Str_arc Irr WU
C.brachiata Thunb. Pol Str_arc Irr WU
C.tangutica (Maxim.)
Korsh.
Pol Str_arc 27.3×26.7 7.5 Pol Str_arc 31.9×24.7 17.2
C.akebioides (Maxim.)
Veitch
Pol Str_arc 29.5×22.6 Pol Str_arc 31.8×23.8
C.glauca Willd. Irr WU Pol Str_arc
C.intricata Bunge Irr WU 28.5×19.5 5.5 Irr WU 25.5×20.8 17.6
C.orientalis L. Pol Str_arc 23.8×18.8 7.0 Pol Str_arc 24.2×17.8 17.5
Naravel-
iopsis
Hand.
_Mazz.
C.smi lacifolia Wall. Pol Str_arc Irr WU
C. fulvicoma Rehd.et
Wils.
Irr WU Irr WU
C.crassipes var.pubipes
W.T.Wang
Pol Str_arc Pol Str_arc
C.tashiroi Maxim. Pol Str_arc Irr WU
Tubulosa
Decne
C.pinnata Maxim. Irr WU Irr Undulate 28.5×21.8 15.0
C.heracleifolia DC. Irr WU Irr Undulate 31.3×21.0 16.7
Viticella
DC
C.patens Morr.et Dec-
ne.
Irr WU Irr WU 30.6×23.0
C.courtoisii Hand.
_Mazz.
Irr Undulate Irr HU 28.0×21.2
C.florida Thunb. Irr Undulate Irr Undulate 26.2×20.4
C.cadmia Buch._Ham.
ex Wall.
Irr WU 27.4×19.0 Irr WU 30.2×22.8
C.huchouensis Tamura Irr WU Irr WU 31.2×21.9 22.0
Viorna
(Reichb.)
Prantl
C.henryi Oliv. Irr Undulate Irr WU 32.5×19.8 23.1
C.urophylla Franch. Irr Undulate Irr HU 28.7×19.1 17.9
C.leschenaultiana DC. Irr WU Irr WU 29.6×21.8
C.buchananiana DC. Irr WU Irr Undulate 29.0×20.6
C.repens Finet et Gag-
nep.
Irr WU Irr WU 25.5×17.5
C.dasyandra Maxim. Irr WU Irr WU 28.4×23.2
C.rehderiana Craib Irr WU Irr Undulate 24.9×25.1 20.7
C.connata DC. Irr WU Irr WU 32.3×20.5 27.4
C.lasiandra Maxim. Irr WU Irr Undulate 32.5×19.8 23.4
C.ranunculoides Franch. Irr WU Irr WU 28.7×19.1 16.5
C.fusca Turcz. Irr WU Irr Undulate 29.6×24.0 20.2
Atragene
(L.)DC.
C.sibirica Mill. Irr WU Irr Undulate
C.macropetala Ledeb. Irr WU Irr WU 28.6×22.8
Bebaeanth-
era Edgew.
C.tosaensis Makino Pol Str_arc Irr WU
Aspidan_
thera
Spach
C.aristata var.occiden-
talis Benth.
Irr Undulate Irr Undulate
C.acapulcensis Hook et
Arn
Pol Str_arc Irr WU
C.dioica L. Pol Str_arc Pol Str_arc
C.gentianoides DC. Irr WU Irr WU
C.glycinoides DC. Irr WU Irr WU
C.ligusticifolia Nutt. Irr WU Irr Undulate
C.pickeringii A.Gray Irr WU Irr WU
Lasiantha
Tamura
C.lasiantha Nutt. Irr WU Irr WU
HU , heavi ly undulate;Irr , Irregular;Pol , polygonal;Str_arc , straight to arched;WU , weakly undulate.
SHI Jing_Hua et al:Leaf Epidermal Feature in Clematis(Ranunculaceae)with Reference to Its Systematic Significance 261
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SHI Jing_Hua et al:Leaf Epidermal Feature in Clematis(Ranunculaceae)with Reference to Its Systematic Significance 263
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SHI Jing_Hua et al:Leaf Epidermal Feature in Clematis(Ranunculaceae)with Reference to Its Systematic Significance 265
→
Figs.1-15. LM photographs of shape of adaxial epidermal cells , pattern of anticlinal walls of leaves.1-8.Polygonal cells with straight
anticlinal walls.1.Anemone flaccida.×160.2.Clematis apiifolia.×160.3.C.chingii.×160.4.C.acapulcensis.×160.5.C.
smilacifolia.×160.6.Pulsatilla chinensis(with stomata).×256.7.Anemone rivularis(with stomata).×256.8.C.intricata (with
stomata).×256.9-15.Irregular cells with weakly undulate anticlinal walls.9.C.heracleifolia.×256.10.C.patens.×200.11.
C.rehderiana.×256.12.C.pickeringii.×160.13.Naravelia pilurifera .×200.14.C.gentianoides(with stomata).×160.15.
C.cadmia (with stomata).×256.
Figs.16-21. LM photographs of shape of upper epidermal cells , pattern of anticlinal walls of leaves.22-30.LM photographs of shape of
lower epidermal cells , pattern of anticlinal walls of leaves.16-20.Irregular cells with undulate anticlinal walls.16.C.lasiantha.×200.
17.C.armandii.×160.18.C.terniflora.×256.19.C.florida.×160.20.C.ligusticifolia(with stomata).×256.21.Irregular
cells with heavily undulate anticlinal walls of C.chinensis.×160.22 , 23.Polygonal cells with straight anticlinal walls.22.C.akebioides.×160.23.C.fruticosa.×200.24-30.Irregular cells with weakly undulate anticlinal walls.24.C.tashiroi.×160.25.C.gen-
tianoides.×160.26.C.brevicaudata.×160.27.C.grandidentata.×160.28.C.fasciculiflora.×160.29.C.acapulcensis.×160.30.N.laurifolia.×256.
Figs.31-45. LM photographs of shape of lower epidermal cells , pattern of anticlinal walls of leaves.31-33.Irregular cells with weakly
undulate anticlinal walls.31.C.ranunculoides.×256.32.C.obscura.×256.33.C.patens.×160.34-42.Irregular cells with
undulate anticlinal walls.34.C.fusca.×200.35.C.florida.×256.36.C.connata .×200.37.C.aristata var.occidentatalis.
×160.38.C.armandii.×160.39.C.terniflora.×256.40.C.ligusticifolia.×200.41.C.lasiantha.×256.42.C.lasian-
dra.×200.43-45.Irregular cells with heavily undulate anticlinal walls.43.C.apiifolia.×160.44.A.flaccida.×160.45.C.
courtoisii.×260.
Figs.46-57. SEM photographs of genus Clematis.46.C.montana.×1 200.47.C.parviloba.×360.48.C.parviloba.×1 200.
49.C.terniflora.×900.50.C.fruticosa.×420.51.C.fruticosa.×1 200.52.C.intricata.×1 500.53.C.heracleifolia.×360.54.C.heracleifolia.×1 500.55.C.heracleifolia.×360.56.C.lasiandra.×1 500.57.C.lasiandra.×360.
Table 3 Intergeneric analy ses(t test)
Genus Anemone Pulsatilla Clematis
Anemone - 2.335 9.418
Pulsati lla 2.335 - 4.452
Clematis 9.418 4.452 -
Pulsatilla and very small in Clematis.These three genera
exhibit close affinity , Anemone is the most primitive and
Clematis the most advanced group.This feature provides
us a clue to a conjecture that in the trib.Anemoneae , the
more primitive the species is , the larger stomata it has.
Within the genus Clematis , the species of sect.
Cheiropsis have comparatively larger stomata than that of
other section.This result supports the viewpoint referring
the sect.Cheiropsis to the most primitive position of this
genus (Wang , 1998;Fu and Hong , 2001;Wu and
Raven , 2001).
3.3 Stomata on both sides
Most taxa we observed have stomata only on the
abaxial side;few species have stomata on both sides(Anemone rivularis , A.demissa , Pulsatilla chinensis ,
P .campanella , P.cernua , Clematis fruticosa , C.to-
mentella , C.tangutica , C.akebioides , C.glauca ,
C.intricata , C.orientalis , C.cadmia , C.gen-
tianoides and C.ligusticifolia).Possessing stomata on
both sides appears in several different groups that are not
very closely related.We conjecture that this character
does not have a monophyletic origin.However , Pulsatilla
chinensis , P .campanella , P.cernua , Clematis fruti-
cosa , C.tomentella , C.tangutica , C.akebioides , C.
glauca , C.intricata , and C.orientalis all possess
polygonal epidermal cells (sometimes irregular with very
weakly undulated anticlinal wall)with stomata on both
sides of leaves.This characteristic is of some significance
in solving systemic problems.
It is not a common feature to have polygonal epider-
mal cells with stomata on both sides.Only three groups
we observed have such characters:the genus of Pulsatil-
la , the subsect.Orientalis Prantl (in sect.Meclatis(Spach)Tamura), and the subsect.Fruticella (in sect.
Fruticella Tamura).Considering the living environment
of the above_mentioned species , we notice that they all
spread mainly in the arid regions of North and Northwest
China.These characters may be associated with their
adaptation to such environment.
Table 4 Analyses within the genus Clematis(t test)
Subgenus Cheiropsis Clematis Fruticella Meclatis Viticella Viorna
Cheiropsis - 5.537 6.575 3.523 4.225 3.463
Clematis 5.537 - 0.926 1.202 1.674 2.413
Fruticella 6.575 0.926 - 0.289 1.158 1.344
Meclatis 3.523 1.202 0.289 - 0.424 0.809
Viticella 4.225 1.674 1.158 0.424 - 0.263
Viorna 3.463 2.413 1.344 0.809 0.263 -
266 植物学报 Acta Botanica Sinica Vol.45 No.3 2003
Table 5 The characters of leaf epidermis under SEM
Taxa
Inner margin of outer stomatal rim
Adaxial epidermis Abaxial epidermis
Cuticular membrane and wax ornamentation
Adaxial epidermis Abaxial epidermis
Anemone davidii Franch. Undulate Smooth Smooth
A.flaccida Fr.S chmidt Undulate Smooth Flakes
A.rivularis Buch._Ham.ex DC. Undulate Undulate Flakes Flakes
A.demissa Hook.f.et Thoms. Undulate Undulate Flakes Flakes
Pulsatilla chinensis(Bunge)Regel Undulate Undulate Striate and f lakes Striate and flakes
P.campanella Fisch.ex Kryl. Undulate Undulate Flakes Flakes
Clematis montana Buch._Ham.ex DC. Nearly smooth Smooth Striate
C.fasciculif lora Franch.ex Kryl. Undulate Flakes Striate and flakes
C.apiifolia var.argentilucida Rehd.et Wi ls. Undulate Striate Flakes
C.chingii W.T.Wang Nearly smooth Smooth Flakes
C.peterae var.trichocarpa W.T.Wang Undulate Flakes Striate
C.brevicaudata DC. Undulate Flakes Striate
C.parvi loba Gardn.et Champ.ex Benth. Nearly smooth Smooth Striate and flakes
C.finetiana Lévl.et Vant. Undulate Flakes Smooth
C.terniflora var.mandshurica(Rapr.)Ohwi Undulate Flakes Striate and flakes
C.obscura Maxim. Undulate Flakes Striate and flakes
C.uncinata Champ.ex Benth. Undulate Flakes Flakes
C.hexapetala Pall. Undulate Smooth Smooth
C.fruticosa Turcz. Nearly smooth Nearly smooth Striate Striate
C.tangutica (Maxim.)Korsh. Nearly smooth Nearly smooth Smooth Smooth
C.intricata Bunge Nearly smooth Nearly smooth Smooth Smooth
C.orientalis L. Nearly smooth Nearly smooth Smooth Smooth
C.pinnata Maxim. Undulate Flakes Striate and flakes
C.heracleifolia DC. Undulate Smooth Striate
C.huchouensis Tamura Undulate Smooth Striate and flakes
C.henryi Oliv. Nearly smooth Smooth Smooth
C.connata DC. Nearly smooth Flakes Striate
C.lasiandra Maxim. Undulate Striate Striate
C.ranunculoides Franch. Undulate Smooth Striate
C.fusca Turcz. Undulate Flakes Flakes
Concerning the sect.Meclatis , different scholars ex-
pressed different approaches.Tamura(1995)treated it as
a section without any subdivision , whereas Wang (2000)
andGrey_Wilson(2000)divided it into two subsections:
subsect.Orientalis and subsect.Wightianae.Morpho-
logically , subsect.Orientalis , which is settled mainly in
North and Northwest China , differs from the subsect.
Wightianae in the following aspects:while the former is
characterized by its yellow and ascending sepals with
lanceolate filaments , the latter has white and spreading
sepals with linear filaments(Wang , 2000).The result of
our study shows that there are differences in leaf epider-
mis between the two subsections , thus supports the view-
point of the division in this section.
A debate still exists on sect.Fruticella.Grey_Wil-
son(2000)placed C.delavayi in the subsect.Fruticel-
la while Wang (Fu and Hong , 2001)considered it as a
member of the subsect.Angustifolia.Based on the leaf
epidermis features , we accept the latter treatment.The
subsect.Fruticella possesses the outstanding characters
mentioned above (i.e.polygonal epidermal cells with
stomata on both sides).But , C.delavayi lacks such
characters , its leaf epidermal feature is similar to the
species in subsect.Angustifolia due to the presence of ir-
regular cells with undulate anticlinal wall and the absence
of stomata on the adaxial side.
Acknowledgements:The authors thank the curators of
the following Herbaria:Herbarium of Institute of Botany ,
The Chinese Academy of Sciences (PE), the United
States National Herbarium(US), Gray Herbarium of Har-
vard University (GH), Herbarium of Missouri Botanical
Garden (MO), for their generosity in providing speci-
mens.We appreciate the valuable advice from Prof.
WANG Wen_Cai and Prof.ZHANG Zhi_Yun.We are in-
debted to Dr.KONG Hong_Zhi and Dr.YANG Dong_Zhi
for their kind help during our research , to Mr.XIAO
Yin_Hou , Mr.YANG Xue_Jian and Ms.WEN Jie for
their assistance on the experiments.We also express our
thanks to Prof.HU Yu_Xi , Prof.LIN Jin_Xing and Prof.
SHEN Shu_Jin for their comments on the manuscript.
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(Managing editor:PENG Dan(intern))
毛茛科铁线莲属的叶表皮特征及其系统学意义
史京华 李良千＊
(中国科学院植物研究所系统与进化植物学重点实验室 , 北京 100093)
摘要: 用光学显微镜和扫描电镜 , 较全面地观察了铁线莲属(Clematis)植物和邻近类群的叶表皮特征 ,并对其系统
学意义进行了讨论。在光学显微镜下 ,观察了铁线莲属 12 组 63 种 5变种及其同族邻近类群 3 属 9 种;在扫描电镜
下 ,观察了铁线莲属 7 组 27种 2 变种及其邻近类群 2 属 6种植物的成熟叶表皮细胞及气孔器的特征。在光学显微
镜下可见:叶表皮细胞形状(表面观)为多边形 、不规则形 ,垂周壁式样为较平直 、浅波状和波状 , 气孔器普遍存在于
下表皮 ,少数种的上表皮也有分布 , 其类型均为无规则型。在扫描电镜下可见:叶片通常具有条纹或有颗粒状或鳞
片状附属物 ,气孔器外拱盖内缘通常为浅波状或近平滑。在黄花铁线莲组(sect.Meclatis(Spach)Tamura)和灌木铁
线莲组(sect.Fruticella Tamura)中 , 叶表皮具有双面气孔器的特征对于组下亚组的划分有一定意义。 并且叶表皮特
征对于一些种的分类学处理也有一定的价值 ,同时也为属下组间的系统进化关系提供了一些线索。
关键词: 毛茛科;铁线莲属;叶表皮;气孔器
中图分类号:Q949.746.5 文献标识码:A 文章编号:0577-7496(2003)03-0257-12
收稿日期:2002-04-25 接收日期:2002-07-19
基金项目:国家自然科学基金(30070059)。
＊通讯作者。 E_mail:
(责任编辑:彭 丹(实习))
268 植物学报 Acta Botanica Sinica Vol.45 No.3 2003