全 文 ：广 西 植 物 Guihaia Jul． 2013，33(4) :528－537 http:/ / journal． gxzw． gxib． cn
DOI:10． 3969 / j． issn． 1000-3142． 2013． 04． 018
张晓霞，张海燕，许为斌，等． 中国凤仙花科植物叶表皮特征及其分类学意义［J］． 广西植物，2013，33(4) :528－537
Zhang XX，Zhang HY，Xu WB，et al． Leaf epidermal characters and their taxonomic significance in Balsaminaceae，China［J］． Guihaia，2013，
33(4) :528－537
Leaf epidermal characters and their taxonomic
significance in Balsaminaceae，China
ZHANG Xiao-Xia1，2，ZHANG Hai-Yan3，XU Wei-Bin4，YU Sheng-Xiang2*
(1． College of Life Sciences，Qufu Normal University，Qufu，Shandong 273165，China;2． State Key Laboratory of Systematic
and Evolutionary Botany，Institute of Botany，Chinese Academy of Sciences，Beijing 100093，China;3． School of Earth
Sciences and Ｒesources，China University of Geosciences，Beijing 100083，China;4． Guangxi Institute of Botany，
Guangxi Zhuang Autonomous Ｒegion and the Chinese Academy of Sciences，Guilin 541006，China )
Abstract:The leaf epidermal characters of 106 field collections representing 36 species within the family Balsaminace-
ae，were investigated with light microscopy． Most epidermal characters were constant within species． These characters
were valuable in clarifying species circumscriptions and relationships between the two Balsaminaceae genera，Impatiens
and Hydrocera． Although abaxial epidermal characters were found to greatly vary between species，the adaxial epidermis
presented much more valuable taxonomic characters． Based on the latter，the species were divided into five groups． Epi-
dermal characters were closely correlated with geographical distribution rather than with gross morphology． Epidermal
characters were found useful in demarcating species but had limited value in infrageneric subdivision． Epidermal charac-
ters appeared to be heavily modified by different environments．
Key words:Balsaminaceae;Impatiens;leaf epidermis;China;taxonomy
中图分类号:Q949． 7 文献标识码:A 文章编号:1000-3142(2013)04-0528-10
中国凤仙花科植物叶表皮特征及其分类学意义
张晓霞1，2，张海燕3，许为斌4，于胜祥2*
(1． 曲阜师范大学 生命科学学院，山东 曲阜 273165;2． 中国科学院 植物研究所 系统与进化植物学国家重点实验室，北京
100093;3． 中国地质大学 地球科学与资源学院，北京 100083;4． 广西壮族自治区
中 国 科 学 院
广西植物研究所，广西 桂林 541006 )
摘 要:利用光学显微镜观察凤仙花科 106 份样本材料、36 种代表植物的叶表皮微形态特征。结果表明:该
科植物叶表皮微形态特征种内稳定，对于种间及属间关系的界定具有重要的分类学价值。上表皮细胞的形状
及垂周壁的式样种间差异明显，各分类群间有明显的界限，是种间界定的重要依据，因此上表皮微形态特征具
有重要的的分类学价值，基于上表皮的微形态特征将研究的 36 种代表植物划分为 5 个类型。下表皮的微形
态特征虽更为多样，种间差异显著，可用于种间界定，但对于属下划分难以提供有价值的性状。该科植物叶表
皮微形态特征与宏观形态特征的相关性较弱，与地理分布格局的相关性较强，关系更为密切。同一地理分布
区域内的种类宏观形态特征虽然差别明显，但叶表皮微形态特征却表现出较强的一致性，这似乎也反映了叶
表皮微形态这一性状受环境饰变的影响比较明显。综上所述，叶表皮微形态特征可为凤仙花科的系统发育，
收稿日期:2012-10-12 修回日期:2013-01-14
基金项目:国家自然科学基金(31170177) ;国家自然科学基金委重大国际合作项目(31110103911) ;中国科学院知识创新工程重要方向性
项目(KSCX2-EW-Z-1)
作者简介:张晓霞(1987-) ，女，山东人，硕士研究生，从事植物分类学研究，(E-mail)zhangqing1928@ 126． com。
* 通讯作者:于胜祥，博士，主要从事植物分类、区系地理及外来入侵种等研究，(E-mail)yushengxiang@ ibcas． ac． cn。
尤其是凤仙花属种间界定提供有价值的分类学佐证。
关键词:凤仙花科;凤仙花属;叶表皮;中国;分类学
The Balsaminaceae is comprised of two genera，Im-
patiens and Hydrocera． Impatiens is a large genus with
around 900 －1 000 species(Grey-Wilson，1980;Chen，
2001;Chen et al．，2007)distributed all around the world
except Australia and south America． Hydrocera is a
small genus with only 2－3 species(Fischer，2004)occur-
ring in wet areas in the tropics． The Balsaminaceae is a
difficult family in angiosperm taxonomy，because of the
large and complex genus，Impatiens． The phylogeny of
the Balsaminaceae，especially Impatiens，and the evolu-
tionary morphologies are not yet well understood． There
has been no single acceptable infrageneric taxonomic
system in Impatiens (Chen，2001)．
Ｒecent studies in molecular systematics indicate
that the Balsaminaceae was embedded in the basal
clades of the Eriales (Soltis et al．，2005)． The
phylogeny of the Balsaminaceae has been discussed in
several papers over recent years． Yuan et al． (2004)
studied the phylogeny and biogeography of the Balsami-
naceae inferred from ITS data;their work showed the
monophyly of the Balsaminaceae，and also suggested the
monophyly of Impatiens，revealing the origin of Impatiens
in Southeast Asia． Janssens et al． (2006)studied the
phylogeny of Impatiens and Hydrocera based on ITS and
atpB-rbcL data． Their results indicated the relationship
of these genera，and also found 14 clades within Impati-
ens． There was great progress in Impatiens phylogeny
based on molecular data rather than morphological char-
acters(Song et al．，2003，2005;Song，2006;Janssens et
al．，2006，2009) ，but few studies had combined molec-
ular data with morphology to discuss the phylogeny of
the Balsaminaceae． Some phylogenies thus lack the sup-
port of morphological characters，and progress with an
infra-genera taxonomic system for Impatiens has thus met
a huge barrier．
In order to clarify the relationships and patterns of
morphological variation among different groups of Impa-
tiens，much work had been done based on morphology，
pollen，seed chromosomes，and molecules(Shimizu et
al．，1985;Song et al．，2003，2005;Song，2006;Cong et
al．，2007;Yu，2008;Gao et al．，2011)． This work has
shown that Impatiens is a natural group with strong dif-
ferentiation． Although there are several obvious phylo-
genic clades in Impatiens，the relationships between the
clades are uncertain．
Leaf characters are constant and not influenced by
whether the plant is dioecious or monoecious，and leaf
epidermal characters have been shown to be important，
not only in identifying the fossil remains of angiosperms
but also in classification(Stace，1984)． These have
been widely used in taxonomic treatments and systematic
studies(Chen et al．，1991;Luo et al．，2001;Ｒen et al．，
2003;Yang et al．，2005;Liu et al．，2011)． Only a few
species within Balsaminaceae have been examined with
the scanning electron microscope(SEM) ，and the results
have had limited taxonomic value(Cong et al．，2007)．
A few species have been examined by light microscope
(LM) ，and as mentioned above，some works have con-
firmed taxonomical value． However，the value of leaf ep-
idermal characters remains unclear． Our aim was to fur-
ther study these，in order to search for new and valuable
taxonomic characters and to clarify the specific circum-
scriptions within Impatiens．
1 Materials and Methods
We used mature leaves fixed in FAA(formalin-
aceto-alcohol ) from 106 field collections and
representing 36 species with the Balsaminaceae(see
Table 1 for details)． The taxa were sampled by
observing the leaf epidermis of different specimens，in-
cluding collections from different regions．
Material for light microscopy was macerated in
35% sodium hypochlorite solution． Pieces of leaf epi-
dermis were stained with safranin-alcohol(50%) ，and
then dehydrated in an ethanol series before being
mounted in Canada balsam． To check the constancy of
epidermal structure，at least five slides were made from
different parts of a single leaf for each taxon． Epidermal
structures were examined and photographed underan O-
9254期 张晓霞等:中国凤仙花科植物叶表皮特征及其分类学意义
lympus DP70 microscope． The stomatal index
Table 1 Source of materials for observation of leaf epidermal micromorphology
Taxon Province Voucher Upper / lower(epidermis)
Shape of
cells
Anticlinal
wall Stomatal type
L /W
(Stomata)
Stomatal
index Plate Group
Hydrocera triflora Hainan Z． Huang 35156 (PE) Upper polygonal Straight or
arched
Anomocytic 1． 20 18． 60% 1． A1 I
Lower Irregular Sinuolate Anomocytic 1． 32 28% 1． A2 I
Impatiens apalophylla Guangxi S． X． Yu 3748 (PE) Upper Irregular Sinuous Absent Absent Absent 2:I1 III
Lower Irregular Sinuate Anomocytic 1． 13 29． 85% 2:I2 III
I． aquatilis Guangxi S． X． Yu 3721 (PE) Upper polygonal Straight Anisocytic Absent Absent 1:C1 I
Lower Irregular Sinuous Anomocytic and anisocytic 1． 35 23． 23% 1:C2 I
I． arguta Yunnan S． X． Yu 4053 (PE) Upper Irregular Sinuolate Absent Absent Absent 3:B1 III
Lower Irregular Sinuate Most anisocytic and a few anomocytic 1． 23 19． 35% 3:B2 III
I． clavigera Guangxi S． X． Yu 3717 (PE) Upper polygonal Substraight Absent Absent Absent 1:E1 I
Lower Irregular Sinuate Anomocytic 1． 34 21． 15% 1:E2 I
I． cornutisepala Guangxi S． X． Yu 4023 (PE) Upper Irregular Sinuolate Anomocytic 1． 25 7． 45% 4:B1 V
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 35 17． 94% 4:B2 V
I． dicentra Guangxi S． X． Yu 4032 (PE) Upper Irregular Sinuate Most anomocytic and a few anisocytic 1． 45 2． 74% 4:F1 V
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 27 36． 09% 4:F2 V
I． paradoxa Hubei S． X． Yu 4093 (PE) Upper Irregular Sinuate Most anomocytic and a few anisocytic 1． 15 3． 33% 4:H1 V
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 31 27． 69% 4:H2 V
I． bodinieri Guangxi S． X． Yu 3733 (PE) Upper Irregular Sinuate Absent Absent Absent 3:D1 IV
Lower Irregular Sinuate Most anomocytic，a few anisocytic
and paracytic
1． 27 18． 92% 3:D2 IV
I． lobulifera Guangxi S． X． Yu 3220 (PE) Upper Irregular Sinuolate Absent Absent Absent 2:A1 II
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 22 24． 49% 2:A2 II
I． hainanensis Hainan S． K． Lau 27038 (PE) Upper Polygonal Substraight Absent Absent Absent 1:B1 I
Lower Irregular Sinuous Most anomocytic and a few anisocytic 1． 42 14． 63% 1:B2 I
I． lateristachys Sichuan S． X． Yu 4084 (PE) Upper Irregular Sinuate Absent Absent Absent 3:I1 IV
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 17 17． 46% 3:I2 IV
I． laxiflora Sichuan S． X． Yu 3987 (PE) Upper Irregular Sinuous Absent Absent Absent 3:F1 IV
Lower Irregular Sinuate Most anisocytic and a few anomocytic 1． 21 14． 29% 3:F2 IV
I． lecomtei Sichuan S． X． Yu 3873 (PE) Upper Irregular Sinuolate Most anomocytic and a few anisocytic 1． 36 5． 63% 4:E1 V
Lower Irregular Sinuate Anomocytic 1． 33 21． 98% 4:E2 V
I． leptocaulon Guangxi S． X． Yu 3681 (PE) Upper Irregular Sinuate Anomocytic 1． 42 2． 86% 4:C1 V
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 21 21． 43% 4:C2 V
I． longialata Sichuan H． N． Qin et al．
17027 (PE)
Upper Irregular Sinuate Most anomocytic and few anisocytic 1． 33 2． 90% 4:D1 V
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 35 17． 07% 4:D2 V
I． macrovexilla Guangxi S． X． Yu 3350 (PE) Upper Irregular Microsinuous
to Sinuolate
Absent Absent Absent 1:H1 II
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 27 17． 5% 1:H2 II
I． malipoensis Guangxi S． X． Yu 4037 (PE) Upper Irregular Sinuous Absent Absent Absent 2:C1 III
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 15 13． 33% 2:C2 III
I． notolophora Sichuan H． N． Qin et al．
17140 (PE)
Upper Irregular Sinuate Absent Absent Absent 4:A1 IV
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 16 12． 12% 4:A2 IV
I． obesa Guangxi S． X． Yu 3775 (PE) Upper Irregular Sinuolate Absent Absent Absent 1:G1 II
Lower Irregular Sinuate Anomocytic and anisocytic 1． 33 18． 33% 1:G2 II
I． omeiana Sichuan S． X． Yu 4083 (PE) Upper Irregular Sinuate Absent Absent Absent 3:H1 IV
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 46 13． 04% 3:H2 IV
I． oxyanthera Sichuan H． N． Qin et al．
17233(PE)
Upper Irregular Sinuolate Absent Absent Absent 2:B1 II
Lower Irregular Sinuolate Anomocytic 1． 31 14． 75% 2:B2 II
I． parvisepala Guangxi S． X． Yu 3754 (PE) Upper polygonal Straight Absent Absent Absent 1:F1 I
Lower Irregular Sinuate Most anomocytic and rare anisocytic 1． 37 17． 78% 1:F2 I
I． platychlaena Sichuan S． X． Yu 4081 (PE) Upper Irregular Sinuolate Anomocytic and anisocytic 1． 38 2． 08% 4:I1 V
Lower Irregular Sinuate Most anisocytic and a few anomocytic 1． 39 14． 04% 4:I2 V
I． potaninii Sichuan H． N． Qin et al．
17189 (PE)
Upper Irregular Sinuous Absent Absent Absent 3:C1 III
Lower Irregular Sinuate Most Anomocytic，a few anisocytic
and rare diacytic
1． 42 20． 93% 3:C2 III
I． pritzelii Hubei S． X． Yu 4092 (PE) Upper Irregular Sinuolate Absent Absent Absent 2:G1 III
Lower Irregular Sinuate Anomocytic and anisocytic 1． 45 17． 24% 2:G2 III
I． pterocaulon Guangxi S． X． Yu 3719 (PE) Upper Irregular Sinuate Absent Absent Absent 4:G1
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 13 21． 57% 4:G2
I． rostellata Sichuan H． N． Qin et al．
17192 (PE)
Upper Irregular Sinuolate Absent Absent Absent 2:F1 III
Lower Irregular Sinuate Anomocytic 1． 21 16． 13% 2:F2 III
I． rubrostriata Guangxi S． X． Yu 3724 (PE) Upper Irregular Substraight or
microsinuous
Absent Absent Absent 1:D1 I
Lower Irregular Sinuous Anomocytic and anisocytic 1． 22 16． 67% 1:D2 I
I． procumbens Guangxi S． X． Yu 3709 (PE) Upper Irregular Sinuolate Absent Absent Absent 2:H1 III
Lower Irregular Sinuate Most anomocytic and non-typical anisocytic 1． 22 23． 26% 2:H2 III
I． spathulata Guangxi S． X． Yu 3763 (PE) Upper Irregular Sinuolate Absent Absent Absent 2:E1 III
Lower Irregular Sinuate Most anomocytic and a few anisocytic 1． 67 31． 82% 2:E2 III
I． tubulosa Guangxi S． X． Yu 3689 (PE) Upper Irregular Sinuolate Absent Absent Absent 3:A1 III
Lower Irregular Sinuate Most anisocytic and a few anomocytic 1． 34 15% 3:A2 III
I． wenshanensis Guangxi S． X． Yu 4044A (PE) Upper Irregular sinuolate Absent Absent Absent 2:D1 III
Lower Irregular Sinuolate to
sinuous
Most anisocytic and a few anomocytic 1． 42 10． 11% 2:D2 III
I． wilsonii Sichuan S． X． Yu 4071 (PE) Upper Irregular Deep sinuous Most anomocytic and a few anisocytic 1． 40 20． 93% 4:G1 V
Lower Irregular Deep sinuous Most anomocytic and a few anisocytic 1． 40 12． 5% 4:G2 V
035 广 西 植 物 33卷
续表1
Taxon Province Voucher Upper / lower(epidermis)
Shape of
cells
Anticlinal
wall Stomatal type
L /W
(Stomata)
Stomatal
index Plate Group
I． wuchengyii Yunnan S． X． Yu 4061 (PE) Upper Irregular Sinuolate Absent Absent Absent 1:I1 II
Lower Irregular Sinuate Anomocytic 1． 41 15． 63% 1:I2 II
I． quadriloba Yunnan H． N． Qin et al．
17027 (PE)
Upper Irregular Sinuous Absent Absent Absent 3:E1 IV
Lower Irregular Sinuate Anomocytic 1． 51 15． 63% 3:E2 IV
(SI)was calculated using the formula:SI = S /(S+E)×
100%，where S=number of stomata per unit area，and E
=number of epidermal cells per same unit area(Dilcher
1974)． Stomatal terminology is based on the
classification proposed by Baranova(1972，1987，1992)
and Dilcher(1974)．
2 Ｒesults and Analysis
Leaf epidermal characters are listed in Table 1．
Stomatal and other epidermal features are constant within
species and are therefore good characters for taxonomy，
especially in clarifying species circumscriptions．
2． 1 Epidermal cells
The epidermal cells of the Balsaminaceae as seen
under LM are usually polygonal or irregular in form，with
anticlinal cell walls sinuous，undulate，and straight to
curved． The patterns of anticlinal cell walls vary
between species． Furthermore，in the same species the
adaxially anticlinal cell walls and the abaxial ones are
obviously different from each other． Straight to curved
cell walls only occur in adaxial epidermis，namely
Hydrocera triflora (Fig． 1:A) ，Impatiens hainanensis
(Fig． 1:B) ，I． aquatilis(Fig． 1:C) ，I． robrustriata(Fig．
1:D) ，I． clavigera (Fig． 1:E) ，and I． parvisepala(Fig．
1:F)． In contrast，abaxial walls are sinuolate to strongly
sinuous，such as in I． macrovexilla(Fig． 1:H) ，I． wens-
hanensis(Fig． 2:D) ，and I． omeiana(Fig． 3:H)．
2． 2 Stomatal apparatus
Stomata are only present on abaxial surfaces in
most species． There are also some species with stomata
on both surfaces，such as I． longialata (Fig． 4:
D) ，I． paradoxa(Fig． 4:H) ，and I． dicentra(Fig． 4:
F)． There are several types of stomata on the same
blade;anomocytic，anisocytic，and paracytic． The ano-
mocytic is the most common type in Balsaminaceae． The
size of stomata and the length /width(L /W)ratio varies
among species． The minimum ratio was 1． 13，found in
I． apalophylla(Fig． 2:I)and I． pterocaulon(Fig． 3:G) ，
and the maximum was 1． 67，in I． spathulata(Fig． 2:
E)． The stomatal index indicates the density of stomata
in per-unit area of epidermis(Dilcher，1974)． The stom-
atal index value for abaxial epidermis is much larger
than for adaxial epidermis if there are stomata on the
adaxial side;there are only a few stomata on the adaxial
surface if they are present at all． On the adaxial surface
the minimum stomatal index value was 2． 08%，found in
I． platychlaena(Fig． 4:I) ，and the maximum was 18．
60%，in H． triflora(Fig． 1:A)． On the abaxial surface
the minimum stomatal index value was 12． 12%，found
in I． notolophora(Fig．:4:A) ;the maximum was 36．
09%，in I． dicenra(Fig． 4:F)．
2． 3 Guard cells and epidermal hairs
Guard cells in Balsaminaceae usually have
elliptical outlines in surface view． The leaves of the
Balsaminaceae are usually entirely glabrous，although a
small number of species have sparse hairs on the adaxial
blade． Occasional epidermal hairs are found，for
example，in I． wuchengyii(Fig． 1:I)．
The following is a key to different groups of species
based on leaf epidermal characters:
1． Adaxial epidermis without stomata
2． Anticlinal cell walls straight or slightly curved 1． Group I………
2． Anticlinal cell walls undulate，sinuolate，or sinuous
3． Anticlinal cell walls undulate 2． Group II……………………
3． Anticlinal cell walls sinuolate，or sinuous
4． Anticlinal cell walls sinuolate 3． Group III…………………
4． Anticlinal cell walls sinuous 4． Group IV…………………
1． Adaxial epidermis with stomata 5． Group V…………………
3 Conclusion and Disscussion
3． 1 Ｒelationships between epidermal features and
gross morphology
The taxa studied show great variation in abaxial ep-
idermal characters in terms of cell shape and stomatal
index;it is difficult to find criteria for subdivision． We
1354期 张晓霞等:中国凤仙花科植物叶表皮特征及其分类学意义
found very limited correlation between epidermal char-
acters and gross morphological characters． Although
species may belong to the same group based on their ep-
idermal characters，their gross morphology allows them to
be readily distinguished． In Group I，for example，
Hydrocera triflora (Fig． 1: A ) has free
petals，berry-shaped fruit，and tricolporate pollen grains．
These characters are different from Impatiens species，
but the species has the same epidermal characters，
straight or slightly curved anticlinal cell walls，as some
Impatiens species，namely I． hainanensis (Fig． 1:
B) ，I． aquatilis(Fig． 1:C) ，I． rubrostriata(Fig． 1:
D) ，I． clavigera(Fig． 1:E) ，and I． parvisepala(Fig． 1:
F)． However，there is also great variation of morphology
among these Impatiens species，except that I． clavigera
and I． parvisepala are close in form． I． hainanensis is
different from I． aquatilis and I． rubrostriata in having
four carpels and many ovules per carpel．
Except Group I，there was limited correlation be-
tween epidermal characters and gross morphology in
Group II，Group III，and Group IV． We found a closer
correlation between epidermal and gross characters in
Group V． In Group V，stomata are present on adaxial
surfaces，in spite of different cell shapes and stomatal
indexes． In this group，the species studied are similar in
morphology，except for I． wilsonii，I． longialata，and I．
leptocaulon． The apices of upper and lower petals of lat-
eral united petals have a long hair-like bristle． The spe-
cies with this character are endemic to China(Hooker，
1908;Chen 2001) ，and include I． paradoxa(Fig． 4:H) ，
I． dicentra(Fig． 4:F) ，and I． lecomtei(Fig． 4:E)． Some
other species in Group V，namely I． wilsonii(Fig． 4:
G) ，I． longialata(Fig． 4:D) ，and I． leptocaulon(Fig． 4:
C) ，are easily distinguished morphologically． The pos-
session of four carpels and one ovule per carpel is char-
acteristic of I． wilsonii． I． longialata is easily distin-
guished by its five carpels and undulate leaf margins．
Five carpels and dentate leaf margins are key features
of I． leptocaulon．
3． 2 Correlation between epidermal characters and
geographical distribution
Epidermal characters are more closely correlated
with geographical distribution than is the gross morphol-
ogy． Different groups have different geographical distri-
bution patterns． In Group I，the species studied have ei-
ther straight or curved anticlinal cell walls，and are con-
fined to the south and southwest of China(Fig． 5:A) ;
Hydrocera triflora and I． hainanensis are only found in
Hainan，I． clavigera and I． parvisepala are found in
southwestern Guangxi． Only I． rubrostriata and I．
aquatilis cover a larger region，but both occur in south-
western China． Of the five groups，Group I have the
most southern distribution． Group II includes only five
Impatiens species in a south-north discontinuous distri-
bution pattern．
In Group III，most species studied are from the
south and central areas of China，and no species extends
to Hainan，southern Guangxi，or southern Guangdong．
This group has the largest distribution(Fig． 5:B) ，and is
indicative of the most common epidermal characters in
Balsaminaceae． In Group IV(Fig． 5:C) ，most species
are found in the montane and subalpine zones of China，
especially on western part of the second step of Chinese
terrain，the eastern slopes of the Qing-Zang plateau．
Some species extend to the borders of the second step
and third step．
The species belonging to Group V are distributed
in the central regions of China with a few species exten-
ding to the northwest(Fig． 5:D)． Species with hair-like
bristles on the apices of lateral united petals are mainly
confined to the high altitudes of the central China and
western Sichuan． The epidermal characters of these spe-
cies are closely correlated with the gross morphological
characters and geographical distribution． Although epi-
dermal characters are correlated with geographical distri-
bution very well in most species，there are also some ge-
ographical‘noises’in Group V． I． leptocaulon and I．
wilsonii，for example，appear to have different morpho-
logical characters，and are readily distinguishable from
I． dicentra and its allies． It seems that epidermal char-
acters may be heavily modified by environmental
factors． Some species with obviously different gross mor-
phologies therefore share the same epidermal characters
and geographical distribution patterns．
3． 3 Ｒelationship between Hydrocera and Impatiens
Hydrocera forms a sister clade to Impatiens within
235 广 西 植 物 33卷
Fig． 1 Micromorphology of the leaf epidermis 1． Adaxial epidermis;2． Abaxial epidermis;A． Hydrocera triflora;B． Impatiens hainanen-
sis;C． I． aquatilis;D． I． rubrostriata;E． I． clavigera;F． I． parvisepala;G． I． obesa;H． I． macrovexilla;I． I． wuchengyii．
Balsaminaceae based on molecular data(Janssens et
al．，2006) ，and I． clavigera and its allies are basal taxa
within Impatiens． This hypothesis is confirmed by the
epidermal characters． In Group I，H． triflora，I． clavig-
era，and its ally I． parvisepala，including the relatively
basal taxon I． hainanensis，are all species with straight
or curved anticlinal cell walls，except that there are sto-
mata on the adaxial surface in H． triflora． Although
3354期 张晓霞等:中国凤仙花科植物叶表皮特征及其分类学意义
Fig． 2 Micromorphology of the leaf epidermis 1． Adaxial epidermis;2． Abaxial epidermis;A． I． lobulifera;B． I． oxyanthera;C． I． mali-
poensis;D． I． wenshanensis;E． I． spathulata;F． I． rostellata;G． I． pritzelii;H． I． procumbens;I． I． apalophylla．
there are also some stomata on the adaxial surface in
Group V species，the majority of these species are em-
bedded in the upper clade in the phylogenic tree of the
family (Yu，2008)． It seems therefore，that in
comparison with whether stomata are present on adaxial
surfaces or not，the characters of the anticlinal cell walls
are very taxonomically valuable．
435 广 西 植 物 33卷
Fig． 3 Micromorphology of the leaf epidermis 1． Adaxial epidermis;2． Abaxial epidermis;A． I． tubulosa;B． I． arguta;C． I． potaninii;
D． I． bodinieri;E． I． quadriloba;F． I． laxiflora;G． I． pterocaulon;H． I． omeiana;I． I． lateristachys．
3． 4 Evidence for species circumscriptions
Variation in epidermal characters on adaxial and
abaxial surfaces is easy to recognise． There is obvious
variation on abaxial surfaces in cell shape and stomatal
index，but it is difficult to summarize these variation pat-
terns． The abaxial epidermal characters are much more
valuable for clarification of species circumscriptions than
for subdivision of the genus Impatiens． The epidermal
5354期 张晓霞等:中国凤仙花科植物叶表皮特征及其分类学意义
Fig． 4 Micromorphology of the leaf epidermis 1． Adaxial epidermis;2． Abaxial epidermis;A． I． notolophora;B． I． cornutisepala;C． I．
leptocaulon;D． I． longialata;E． I． lecomtei;F． I． dicentra;G． I． wilsonii;H． I． paradoxa;I． I． platychlaena．
characters on adaxial surfaces provide a much more val-
uable message in species demarcation than those on the
abaxial surface． In addition，the adaxial epidermal char-
acters are correlated with geographical patterns and
gross morphologies．
Acknowledgements We are much indebted to
Dr． Yuan-tong Hou and Dr． O． O． Oyesiku who
critically read the manuscript and kindly helped us in
635 广 西 植 物 33卷
Fig． 5 Geographical distribution patterns with the Balsaminaceae A． GroupⅠ(⊙)and GroupⅡ( ) ;B． GroupⅢ(▲) ;C． GroupⅣ
(★) ;D． GroupⅤ(●)．
its preparation．
Ｒeferences:
Baranova M． 1972． Systematic anatomy of the leaf epidermis in the
Magnoliaceae and some related families［J］． Taxon，21:447－469
Baranova M． 1987． Historical development of the present classifica-
tion of morphological types of stomata［J］． Bot Ｒev，53:53－79
Baranova M． 1992． Principles of comparative stomatographic
studies of flowering plants［J］． Bot Ｒev，58:1－99
Chen YL，Akiyama S，Ohba H． 2007． Balsaminaceae． In:Wu ZY，
Ｒaven PH eds． Flora of China［M］． Beijing:Science Press ＆
St． Louis:Missouri Botanical Garden Press:12:43－113
Chen YL． 2001． Flora of China［M］． Beijing:Science Press:47
(2) :1－243
Chen ZD，Zhang ZY． 1991． A study on foliar epidermis in Betu-
laceae［J］． Acta Phytotax Sin，29(2) :156－163
Cong YY，Liu KM，Chen W，et al． 2007． A study on
microphological characters of leaf epidermis of six species in Im-
patiens L．［J］． J Nat Sci HNU，30(1) :68－71
Dilcher DL． 1974． Approaches to the identification of angiosperm
leaf remains［J］． Bot Ｒev，40:1－157
Fischer E． 2004． Balsaminaceae Kubitzki K(ed)． The Families
and Genera of Vascular Plants［M］，Berlin:Springer:6:20－25
Gao M，Xu WB，Yu SX，et al． 2011． Characters of leaf epidermis and
their taxonomic significance in Impatiens(Balsaminaceae)obligated
to limestone region from China［J］． Guihaia，31(6):730－734
Grey-Wilson C． 1980． Impatiens of Africa［D］． Ｒotterdam:A． A．
Balkema:1－59
Hooker JD． 1908． Les especes du genre“Impatiens”dans I’
herbier du Museum de Paris［J］． Nov Arch Mus Nat Hist Paris，
10(4) :233－272
Janssens SB，Knox E B，Huysmans S，et al． 2009． Ｒapid radiation
of Impatiens(Balsaminaceae)during Pliocene and Pleistocene:
result of a global climate change［J］． Mol Phylogen Evol，52:
806－824
Janssens SB，Geuten K，Yuan YM，et al． 2006． Phylogenetics of
Impatiens and Hydrocera (Balsaminaceae)using chloroplast
atpB-rbcL spacer sequences［J］． Syst Bot，31:171－180
Liu W，Zhu XY． 2011． Leaf epidermal characters and taxonomic
revision of Schizophragma and Pileostsgia (Hydrangeaceae)
［J］． Bot J Linn Soc，165:285－314
Luo Y，Zhou ZK． 2001． Leaf epidermis of Quercus subgen． Cy-
clobalanopsis (Oerst．)Schneid．(Fagaceae) ［J］． Acta Phytotax
Sin，39(6) :489－501
Ｒen H，Pan KY，Chen ZD，et al． 2003． Structural characters of
leaf epidermis and their systematic significance in Vitaceae［J］．
Acta Phytotax Sin，41(6) :531－544
Shimizu T，Takao S． 1985． Taxonomic discussions on the four-car-
pellate species of Impatiens(Balsaminaceae) ［J］． Acta Phytotax
Geobot，36:97－106
Soltis DE，Soltis PS，Endress PK，et al． 2005． Phylogeny and Evo-
lution of Angiosperms［M］． Sunderland:Sinauer Associates，
Inc． Publishers
Song Y，Yuan YM，Küpfer P． 2003． Chromosomal evolution in
Balsaminaceae with cytological observations on 45 species from
southeast Asia［J］． Caryologia，56:463－481
Song Y，Yuan YM，Küpfer P． 2005． Seedcoat micromorphology of
Impatiens(Balsaminaceae)from China［J］． Bot J Linn Soc，
149:195－208
Song Y． 2006． Evolution and biogeography of Balsaminaceae:in-
sights from molecular phylogeny［D］． Neuchtel:University of
Neuchtel-Faculty
Stace CA． 1984． The Taxonomic Importance of the Leaf Surface
［M］． In:Heywood VH，Moore DM (eds)． Current concepts in
plant taxonomy． London:Academic Press:25:67－94
Yang ZＲ，Lin Q． 2005． Comparative morphology of the leaf epidermis
in Schisandra(Schisandraceae)［J］． Bot J Linn Soc，148:39－56
Yu SX． 2008． Ｒevision of Impatiens L．(Balsaminaceae)in Guan-
gxi，with a study on the phylogeny of the genus in China［D］．
Beijing:Chinese Academy of Sciences
Yuan YM，Song Y，Geuten K，et al． 2004． Phylogeny and biogeog-
raphy of Balsaminaceae inferred from ITS sequence data［J］．
Taxon，53:391－403
7354期 张晓霞等:中国凤仙花科植物叶表皮特征及其分类学意义