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Epidermal characters of Tamarix L.(Tamaricaceae)from Northwest China and their taxonomic and palaeogeographic implications

更新时间:2016-07-05

1. Introduction

The genus Tamarix L.(Tamaricaceae)with about 90 species is a salt-and alkali-tolerant plant,forming evergreen or deciduous shrubs or trees with scale-like leaves,discontinuously distributed in the arid and semi-arid areas of Eurasia,Africa and around the coast of the ancient Mediterranean Sea(Baum,1978;Liu et al.,2012;Yang and Gaskin,2007;Yin,1995).China is considered to be the secondary center of origin of Tamarix,containing 18—20 species,which are mainly distributed in the northwestern area,in Xinjiang,Qinghai,Gansu,Ningxia and Inner Mongolia(Liu et al.,2012;Pan,1998;Yin and Yang,1998;Zhang and Liu,1988).Among these species,nearly 45 percent(8/18)are locally endemic.The species of Tamarix from northwestern China show similarity in gross morphologies,such as slender,smooth and reddish—brown branches and grey—green foliage,thus,they lack clear and obvious taxonomical characters(Zhang,2004a,2005;Zhang et al.,2002).As such,identification,systematic position and relationships of the species are uncertain and have been widely discussed(Cheng et al.,2000;Feng and Yin,2000;Hua et al.,2004;Wei et al.,1999;Yang and Gaskin,2007;Zhang,2004a,2005;Zhang et al.,2000,2002).

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Based on the extant distribution,the fossil record and the palaeogeography,the genus Tamarix probably originated in the Eocene,in coastal areas of the ancient Mediterranean Sea,and its ancestors thrived under warm and humid climatic conditions(Li et al.,2012;Zhang et al.,2003a).After the Miocene,with the retreat of the ancient Tethys Sea,the genus spreads eastwards,and some representatives extended to China via the Central Asia Region(Zhang et al.,2003a).During this diffusion,differentiation occurred as adaptations to the arid and cool climates(Zhang et al.,2003a).

The taxonomical research of Chinese Tamarix dates back to the 18th century(Loureiro,1790).In recent years,such kind of studies has been carried out indepth,focusing on leaf and flower morphology and anatomy(Feng and Yin,2000;Liu et al.,2012;Wei et al.,1999;Yang and Gaskin,2007;Zhai et al.,1983;Zhang,2004a;Zhang et al.,2003b),seed and pollen morphology(Xi,1988;Zhang,2004b;Zhang et al.,1998,2001),chromosome number(Zhai and Li,1986),phytochemistry(Cheng et al.,2000)and molecular aspects(Gaskin et al.,2004;Hua et al.,2004;Zhang et al.,2000).However,the taxonomical position of some species,e.g.,Tamarix albiflonum M.T.Liu and Tamarix korolkowi Rgel&Schmalh.,is still being questioned(Liu et al.,2012;Yang and Gaskin,2007).Because of their morphological similarity and natural hybridization,some species,e.g.,Tamarix ramosissima Ledeb.,T.korolkowi,Tamarix tarimensis P.Y.Zhang&M.T.Liu,Tamarix arceuthoides Bunge and Tamarix hohenackeri Bunge are difficult to distinguish(Zhang,2004a;Zhang and Zhang,1990).Even the extinction of some species,such as Tamarix jintaensis Zhang et Liu and Tamarix sachensis Zhang et Liu,is doubted(Pan,1998;Wang and Yin,2004;Yang et al.,2002;Yin,2002).Thus,the species in China lack a unified and widely accepted system of classification(Feng and Yin,2000;Hua et al.,2004;Liu et al.,2012;Yang and Gaskin,2007;Zhang,2004a,2005;Zhang and Zhang,1990;Zhang et al.,2002,2003b).Tamarix is a genus with highly chaotic classification(Hua et al.,2004;Xun et al.,2007;Zhang,2004a;Zhang et al.,2002).As to the systematics,the phylogenetic relation ship of the species is also not clear.In the studies of the 16 species from China,Hua et al.(2004)and Zhang(2004a)have given controversial results based on either morphological characters or molecular data.

自2012年国内磷复肥表观消费量达到峰值以来,中国磷复肥行业开始进入供给侧结构性改革的大周期,行业发展从量的充足向质的提升转型。面对问题与困难,国内磷复肥企业积极去产能、调结构、提高核心竞争力,不断培育新的增长点,着重发展适应农业发展需求的差异化、环保高效的新型肥料,线上线下并举持续推动服务下沉,逐步缓解了产能过剩的压力,促进了化肥供需平衡,推动了国内市场的理性成熟,使行业技术水平更上层楼,盈利能力整体回暖。

Foliar epidermal characters,such as epidermal cells,stomata,trichomes and salt glands,have been used as taxonomic and phylogenetic features among the angiosperms(Abbruzzese et al.,2013;Baranova,1987,1992;Gupta and Murty,1984;Jones,1986;Wang et al.,2015).Currently,studies of leaf epidermal characters of Tamarix are relatively rare.Gupta and Murty(1984)have described the leaf epidermal structures in some species of Tamaricaceae.Lately,Abbruzzese et al.(2013)and Kuzminsky et al.(2014)have studied the epidermal morphology of Tamarix africana Poiret and Tamarix gallica Linnaeus from southern Italy.Alaimo et al.(2013)also studied the leaf anatomy of Tamarix arborea var.arborea.In China,Zhai et al.(1983)have described some general structures of leaf epidermis,and Zhang et al.(2003b)have studied some epidermal features of young branches from 16 species.

In the present paper,we report the leaf epidermal characters of 17 species from China.The micromorphological features of epidermal cells,stomata,salt glands,papillae and epidermal hairs of both adaxial and abaxial epidermis are described.Based on these epidermal variations,the taxonomical position and systematic relationships among species of Tamarix are discussed.

Based on the above discussion,T.ramosissima,T.tarimensis,T.arceuthoides and T.hohenackeri are closely related genetically.The variations between them probably are intraspecific.Therefore,we consider T.tarimensis,T.arceuthoides and T.hohenackeri as variants of T.ramosissima:T.ramosissima var.tarimensis,T.ramosissima var.arceuthoides and T.ramosissima var.hohenackeri.

2. Material and methods

2.1. Selection of the extant species in China

成语中的宾语前置,经常以助词“是”为标记。“惟命是从”的意思是一定要服从接受到的命令,不可以有一点违背的情况。宾语“命”前置在谓语“从”的前面。类似的现象在成语中还有很多,比如“惟利是图 ”中的“利”、“马首是瞻”中的“马首”、“惟才是举”中的“才”等都是“是”字前面的宾语。

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2.2. Group of the species

In the Chinese species of genus Tamarix,two types of flowers have been found—the four-merous flower,which means there are four petals in a flower,and the five-merous flower,which means there are five petals in a flower.Then,the 17 species are grouped on the basis of their flower:The first group includes the species which only have four-merous flowers;the second group includes the species which onlyhave five-merous flowers;a third group includes those species which have both four-merous and five-merous flowers.

2.3. Study method of leaf epidermis

The growing branches with leaves have been immersed in 20%CrO3solution for 48—72 h,according to the standard protocols(Alvin and Boulter,1974;Kerp,1990).The epidermis of scale-like leaves have been watered,cleaned with 50%alcohol and peeled under a Leica S8APO stereoscope microscope.About 50 leaves of each species have been prepared.The leaf epidermis was then stained in 0.5%safranine solution,mounted on microscope slides and observed under an Olympus BX51 stereomicroscope and photographed with a PixeLINK Megapixel FireWire Camera(DSC-600).The leaf epidermis was also mounted on a scanning stake and photographed under a Zeiss Supra-55VP scanning electron microscope.

3. Results

3.1. General leaf epidermal characters

The three species,Tamarix elongata,T.laxa and Tamarix androssowii,only have four-merous flowers.T.androssowii Litv.is distinguishable from T.elongata Ledeb.and T.laxa Willd.by the undulated cell walls on the adaxial epidermis(Fig.1m and o),since the latter two species have only straight cell walls(Fig.1a,c,g,i);the papillae on the adaxial epidermis of T.androssowii are slender(height of papilla is smaller compared to width;Fig.1q),while they are stout(height of papilla nearly equal to or a bit larger than its width)in T.elongata and T.laxa(Table 2;Fig.1e and k),that is,the height of the papilla is distinguishable.T.elongata differs from T.laxa typically in the short,round and isodiametric cells on the abaxial epidermis(Fig.1f),since the cells on the abaxial epidermis of T.laxa are quadrangular and elongated(Fig.1l).

Table 1 Species of the genus Tamarix from the Herbarium of Turpan Eremophytes Botanical Garden,Chinese Academy of Sciences(CAS),Turpan,Xinjiang,Northwest China.

Tamarix species Specimen No. Identified by and date Collection sites T.elongata Ledeb. 00075400 M.T.Liu,13/7/2009 Yanqi(Qarasahr)County,Xinjiang T.laxa Willd. 00021365 M.T.Liu,4/1/1988 Cele(Qira)County,Xinjiang T.androssowii Litv. 00080 M.T.Liu,21/12/1977 Minle County,Gansu T.taklamakanensis M.T.Liu 00075448 M.T.Liu,27/1/1981 Lop Nor,Xinjiang T.albiflonum M.T.Liu —— Turpan Eremophytes Botanical Garden,CAS T.austromongolica Nakai 002287 M.T.Liu,30/8/1978 Bayannuur,Inner Mongolia T.chinensis Lour. 00097 M.T.Liu,29/1/1978 Zhanhua County,Shandong T.leptostachya Bunge 00075349 M.T.Liu,13/7/2009 Shihezi City,Xinjiang T.karelinii Bunge 00075433 M.T.Liu,20/8/1978 Qaidam Basin,Qinghai T.hispida Willd. 00079615 M.T.Liu,13/7/2009 Zhongwei County,Ningxia T.ramosissima Ledeb. 00079616 M.T.Liu,13/7/2009 Zhongwei County,Ningxia T.korolkowi Rgel&Schmalh. 0055144 M.T.Liu,2/9/1978 Aksu City,Xinjiang T.tarimensis P.Y.Zhang&M.T.Liu 00075429 Krym,14/12/1999 Minfeng County,Xinjiang T.arceuthoides Bunge 00075405 M.T.Liu,13/9/2009 Wusu City,Xinjiang T.hohenackeri Bunge 00075417 M.T.Liu,13/7/2009 Hami City,Xinjiang T.gracilis Willd. 002291 M.T.Liu,5/8/1978 Minle County,Gansu T.gansuensis H.Z.Zhang ex P.Y.Zhang&M.T.Liu 00078 M.T.Liu,30/8/1978 Aksu City,Xinjiang

Table 2 Leaf epidermal characters of species of the genus Tamarix from China.

3.2. Leaf epidermal character variation in species with four-merous flower

The leaves of Tamarix from China are bifacial with stomata and salt glands distributed on both adaxial and abaxial epidermis(Table 2).The cells on both adaxial and abaxial epidermis are polygonal,isodiametric,round or irregular in shape,and their anticlinal walls are undulated or straight on the adaxial epidermis,but straight on the abaxial epidermis.The cells on the adaxial epidermis are slightly smaller and regularly arranged in longitudinal files,while they are slightly larger,and mostly irregularly arranged on the abaxial epidermis.The adaxial epidermis is usually strongly papillate or covered with epidermal hairs;while the abaxial epidermis is flat,swollen,papillate or covered with epidermal hairs.The salt glands are round in shape,irregularly arranged,raised or sunken on the adaxialepidermis,but sunken on the abaxial epidermis.The stomata are oblong-or spindle-shaped,smaller than the glands,sunken on both adaxial and abaxial epidermis, and mostly their long axes are nearly vertical to the long axis of the leaves.

3.3. Leaf epidermal character variation in species with five-merous flower

Some plants from China were considered to be T.korolkowi,which has been described from Russian and Central Asia(Liu,1994;Liu et al.,2012).Zhang and Zhang(1990)discussed these plants based on the morphological similarities to T.ramosissima or T.leptostachya,and thought the Chinese T.korolkowi could be a hybrid of T.ramosissima and T.leptostachya.Based on our studies,T.korolkowi shows minimal differences with T.ramosissima in epidermal characters(Table 2),and their common features include the undulated cell walls on the adaxial epidermis(Fig.3o and u)and the ‘wall’-like structure occurring between cell files on the abaxial epidermis(Fig.3r and x).Thus,we agree with Zhang and Zhang(1990)and also consider the Chinese T.korolkowiasa synonym of T.ramosissima.

Among them,the three species of T.taklamakanensis M.T.Liu,T.albiflonum and T.austromongolica Nakai have flat abaxial epidermis,that is,their abaxial epidermis lacks papillae or epidermal hair(Figs.1x and 2f,l).T.taklamakanensis is distinguishable from T.albiflonum and T.austromongolica in the adaxial epidermis,which is flat and lacks papillae or epidermal hair(Fig.1w),while in the latter two species,the adaxial epidermis is swollen and has papillae or epidermal hairs(Fig.2e and k).T.albiflonum differs fromT. austromongolica in the irregularly arranged cells (Fig. 2a and c) and the stout papillae (Fig. 2e) on the adaxial epidermis; since in T. austromongolica, cells are regularly arranged (Fig. 2g and i) and papillae elongated to epidermal hairs (Fig. 2k) on the adaxial epidermis.

The other nine species,T.chinensis Lour.,T.leptostachya Bunge,T.karelinii Bunge,T.hispida Willd.,T.ramosissima,T.korolkowi,T. tarimensis,T.arceuthoides and T.hohenackeri,have swollen abaxial epidermis,that is,their abaxial epidermis is clearly papillate or has epidermal hairs.

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In species of T.chinensis(Fig.2q),T.leptostachya(Fig.2w)and T.karelinii(Fig.3e),the papillae on the adaxial epidermis are stout and not elongated.T.karelinii can be distinguished from T.chinensis and T.leptostachya by the comparatively flatter abaxial epidermis,which has fewer papillae(Fig.3f),while the abaxial epidermis of T.chinensis and T.leptostachya is clearly swollen and densely papillate(Fig.2r and x).T.chinensis differs from T.leptostachya in the polygonal cells on the abaxial epidermis(Fig.2p and r),which are spindle-shaped in T.leptostachya(Fig.2v and x).

定理3.2 设(X,τ)为拓扑空间,U∈τ,U为CSI-开当且仅当对X中的任意可数既约闭集A,若Aδ∩U≠Ø,则A∩U≠Ø。

3.4. Leaf epidermal character variation in species with both four-merous and five-merous flower

Fig.1 Leaf epidermal characters of Tamarix from China:a—f— Tamarix elongata;g—l— Tamarix laxa;m—r— Tamarix androssowii;s—x—Tamarix taklamakanensis.a—b,g—h,m—n,s—t— Light micrographs,scale bar=200 μm;a,g,m,s— Adaxial epidermis;b,h,n,t— Abaxial epidermis.c—f,i—l,o—r,u—x — Scanning electron micrographs,scale bar=40 μm;c,i,o,u — Adaxial epidermis,inner surface;d,j,p,v —Abaxial epidermis,inner surface;e,k,q,w—Adaxial epidermis,outer surface;f,l,r,x—Abaxial epidermis,outer surface.Arrow 1—A cell,round,anticlinal walls straight;Arrow 2—A stoma,oblong or spindle-shaped,long axis nearly vertical to long axis of the leaf;Arrow 3—A cell,strongly concave,periclinal wall with a pit;Arrow 4—A salt gland,round,larger than stoma;Arrow 5—A papilla,stout and ball-shaped;Arrow 6—A salt gland,sunken;Arrow 7—A cell,surface flat or slightly swollen,lacking papilla;Arrow 8—A cell,slightly elongated,anticlinal walls straight;Arrow 9—A salt gland,irregularly arranged;Arrow 10—A salt gland,raised;Arrow 11—A cell,surface flat or slightly swollen,lacking papilla;Arrow 12—A salt gland,sunken;Arrow 13—A cell,anticlinal walls undulated;Arrow 14—A cell,slightly concave or having straight periclinal walls;Arrow 15—A fine papilla,slender;Arrow 16—An epidermal surface, flat,lacking papilla or epidermal hair;Arrow 17—A salt gland,raised;Arrow 18—An epidermal surface flat,lacking papilla or epidermal hair.

Tamarix gracilis Willd.shows the adaxial epidermis papillate and the papillae stout(Fig.4w)and the abaxial epidermis flat or slightly papillate(Fig.4x).Thus,T.gracilis is more similar to the species with four-merous flower(Table 2).Tamarix gansuensis H.Z.Zhang ex P.Y.Zhang&M.T.Liu has the adaxial epidermis covered with the epidermal hairs(Fig.5e),and the abaxial epidermis covered with stout papillae(Fig.5f),thus being more similar to T.ramosissima,T.korolkowi,T. tarimensis,T.arceuthoides and T.hohenackeri among species with five-merous flower.T.gracilis can be distinguished from T.gansuensis by the wedge-shaped epidermal cells on the abaxial epidermis(Fig.4x).

4. Discussion

4.1. Taxonomic implication

Although T.albiflonum is unique by its white flowers(Liu,1994;Liu et al.,2012),this species has been confused with T.androssowii for a long time(Yang and Gaskin,2007;Zhang and Zhang,1990).Based on our studies,T.albiflonum differs distinctly from T.androssowii in epidermal characters.In T.albiflonum,the cells are irregularly arranged with straight walls on the adaxial epidermis(Fig.2a and c),while they are regularly arranged in files with undulated walls in T.androssowii(Fig.1m and o);the papillae on the adaxial epidermis of T.albiflonum are stout(Fig.2e),while they are slender in T.androssowii(Fig.1q).Besides,on account of the above descriptions(Table 2),T.albiflonum also clearly differs from other species in China.Thus,our studies consolidate the establishment of this species.

The twelve species,Tamarix taklamakanensis,T.albiflonum,Tamarix austromongolica,Tamarix chinensis,Tamarix leptostachya,Tamarix karelinii,Tamarix hispida,T.ramosissima,T.korolkowii, T.arceuthoides,T.tarimensis and T.hohenackeri,only have five-merous flowers.

Based on the above descriptions,T.ramosissima,T.tarimensis,T.arceuthoides and T.hohenackeri are very similar in epidermal characters.Their cells are polygonal,isodiametric or irregular in shape;their adaxial epidermis is strongly papillate,and the papillae are elongated to short epidermal hairs(Figs.3q and 4e,k,q);their abaxial epidermis is swollen,and the papillae are stout,ball-shaped and not elongated(Figs.3r and 4f,l,r).These four species only differ slightly in the cell walls and the epidermal hairs on the adaxial epidermis,and the thickened cell walls on the abaxial epidermis(Table 2).Morphologically,T.ramosissima ,T.tarimensis,T.arceuthoides and T.hohenackeri also show close similarities in the flower merous,the length of racemes,the shape and length of petals and sepals,the size of capsule,and the shape and size of leaves and bracts(Table 3).T.tarimensis and T.hohenackeri differ from T.ramosissima by the smaller leave size;Tamarix arceuthoides differs from T.ramosissima in possessing longer racemes and smaller leaves and bracts,and petals of the former are completely open and deciduous after anthesis than half open and persistent in fruit as in the case of the latter(Table 3).Besides,the three species T.ramosissima,T.arceuthoides and T.hohenackeri can be hybridized among themselves(Liu et al.,2012;Zhang and Zhang,1990).

生态足迹和生态承载力的计算结果可以生态账户形式体现并初步判断研究区生态盈余的状态[14],其计算公式为:

Eighteen species and two variants of Tamarix are recordedfrom China(Yang and Gaskin,2007;Zhangand Zhang,1990).In the recent publication by Liu et al.(2012),two species,T.albiflonum and T.korolkowi,are also added to the subregion of China.Among these species,Tamarix aphylla(Linnaeus)Karsten which is only cultivated in Taiwan of China(Yang and Gaskin,2007;Zhang and Zhang,1990),is not included in this study.T.jintaensis,T.sachensis and Tamarix laxaWilld.var.polystachya(Ledeb.)Bunge were not available for study,some of them are doubted to be extinct(pers.comm.Prof.Bo-Rong Pan).The 17 species in the current study are listed in Table 1.

4.2. Taxonomic treatment

Tamarix ramosissima var.ramosissima Ledeb.≡Tamarix ramosissima Ledeb., Flora Altaica[Ledebour](1829)424;Flora Orientalis[Boissier](1867)776;Taxon[Villar](2014)1140.

Inspeciesof T.hispida,T.ramosissima,T.korolkowi,T.tarimensis,T.arceuthoides and T.hohenackeri,the papillae on the adaxial epidermis are elongated to long or short epidermal hairs(Figs.3k,q,w and 4e,k,q).T.hispida is distinguishable by the long epidermal hairs on both the adaxial and abaxial epidermis(Fig.3k and l),while in the other five species,the adaxial epidermis has short epidermal hairs(Figs.3q,w and 4e,k,q),and the abaxial epidermis has stout papillae(Figs.3r,xand4f,l,r).T.ramosissima and T.korolkowi show minimal difference inepidermal characters;but they differ from T.tarimensis,T.arceuthoides and T.hohenackeritypically in the ‘wall’-like structure occurring between cell files on the abaxial epidermis(Fig.3r and x),since in the latter three species,the abaxial epidermis has no‘wall’-like structure(Fig.4f,l,r).T.tarimensis differs slightly from T.arceuthoides and T.hohenackeri in the straight cell walls on the adaxial epidermis(Fig.4c),since the latter two species have only undulated cell walls(Fig.4i and o).T.arceuthoides differs from T.hohenackeri by the clearly elongated epidermal hairson the adaxial epidermis(Fig.4k),since the epidermal hairs in T.hohenackeri are shorter(Fig.4q).

Tamarix ramosissima var.tarimensis(P.Y.Zhang&M.T.Liu)J.W.Zhang&B.R.Pan,comb.nov.≡Tamarix tarimensis P.Y.Zhang&M.T.Liu,Acta Bot Boreal-Occid Sin[Zhang](1988)263.

Tamarix ramosissima var.arceuthoides(Bunge)J.W.Zhang&B.R.Pan,comb.nov.≡Tamarix arceuthoides Bunge,Mém Acad Imp Sci St-Pétersbourg Divers Savans[Bunge](1851)295;Beitr Fl Russl[Bunge](1852a)119.

Tamarix ramosissima var.hohenackeri(Bunge)J.W.Zhang&B.R.Pan,comb.nov.≡Tamarix hohenackeri Bunge,Tent Gen Tamar[Bunge](1852b)44.

Fig.2 Leaf epidermal characters of Tamarix from China:a—f—Tamarix albiflonum;g—l— T.austromongolica;m—r— T.chinensis;s—x— T.leptostachya.a—b,g—h,m—n,s—t—Light micrographs,scale bar=200 μm;a,g,m,s—Adaxial epidermis;b,h,n,t—Abaxial epidermis.c—f,i—l,o—r,u—x— Scanning electron micrographs,scale bar=40 μm;c,i,o,u — Adaxial epidermis,inner surface;d,j,p,v— Abaxial epidermis,inner surface;e,k,q,w—Adaxial epidermis,outer surface;f,l,r,x—Abaxial epidermis,outer surface.Arrow 1—Cells,irregularly arranged;Arrow 2—A papilla,stout and ball-shaped;Arrow 3—Epidermal surface, flat,lacking papilla or epidermal hair;Arrow 4—Cells,elongated,regularly arranged in files;Arrow 5—Epidermal surface, flat,lacking papilla or epidermal hair;Arrow 6—A papilla,stout and ball-shaped;Arrow 7—A papilla,stout and ball-shaped;Arrow 8—Cell with anticlinal walls,straight or undulated;Arrow 9—Cells,slightly concave;Arrow 10—A salt gland,sunken;Arrow 11—A papilla,stout and ball-shaped,and cell,spindle-shaped.

Fig.3 Leaf epidermal characters of Tamarix from China:a—f—Tamarix karelinii;g—l—T.hispida;m—r—T.ramosissima;s—x—T.korolkowi.a—b,g—h,m—n,s—t—Lightmicrographs,scalebar=200μm;a,g,m,s—Adaxialepidermis;b,h,n,t—Abaxialepidermis.c—f,i—l,o—r,u—x—Scanning electron micrographs,scale bar=40 μm;c,i,o,u —Adaxial epidermis,inner surface;d,j,p,v— Abaxial epidermis,inner surface;e,k,q,w—Adaxialepidermis,outersurface;f,l,r,x—Abaxialepidermis,outersurface.Arrow1—Acell,round;Arrow2—Acell,concave;Arrow 3—A papilla,stout;Arrow 4—A salt gland,sunken;Arrow 5—A papilla,stout and ball-shaped;Arrow 6—A cell,concave;Arrow 7—A long epidermal hair;Arrow 8—A papilla,elongated to long epidermal hair;Arrow 9—A cell,anticlinal walls undulated;Arrow 10—A cell,slightly concave or having straight periclinal walls;Arrow 11—An epidermal hair;Arrow 12—A salt gland,raised;Arrow 13—Swollen epidermal surface,stout and round papillae;Arrow 14 —‘Wall’-like structure between cell files;Arrow 15—A cell,anticlinal walls undulated;Arrow 16—A cell,slightly concave or having straight periclinal walls;Arrow 17 — A salt gland,raised;Arrow 18 — ‘Wall’-like structure occurring between cell files.

Fig.4 Leaf epidermal characters of Tamarix from China:a—f— Tamarix arceuthoides;g—l— T.tarimensis;m—r— T.hohenackeri;s—x— T.gracilis.a—b,g—h,m—n,s—t— Light micrographs,scale bar=200 μm;a,g,m,s— Adaxial epidermis;b,h,n,t—Abaxial epidermis.c—f,i—l,o—r,u—x— Scanning electron micrographs,scale bar=40 μm;c,i,o,u — Adaxial epidermis,inner surface;d,j,p,v— Abaxial epidermis,inner surface;e,k,q,w—Adaxial epidermis,outer surface;f,l,r,x—Abaxial epidermis,outer surface.Arrow 1—A cell,anticlinal walls straight;Arrow 2—A cell,slightly concave;Arrow 3—A salt gland,raised;Arrow 4—An epidermal hair;Arrow 5—A cell,surface swollen;Arrow 6—A cell,anticlinal walls undulated;Arrow 7—A salt gland,raised;Arrow 8—A cell,surface swollen;Arrow 9—A cell,anticlinal walls undulated;Arrow 10—A short epidermal hair;Arrow 11—A cell,surface swollen;Arrow 12—A cell,concave;Arrow 13—A papilla,stout,round and ball-shaped;Arrow 14—A salt gland,sunken;Arrow 15—A wedge-shaped cell,surface flat,lacking papilla or epidermal hair.

Fig.5 Leaf epidermal characters of Tamarix from China:a—f — Tamarix gansuensis.a—b — Light micrographs,scale bar=200 μm;a —Adaxial epidermis;b —Abaxial epidermis.c—f— Scanning electron micrographs,scale bar=40 μm;c—Adaxial epidermis,inner surface;d —Abaxial epidermis,inner surface;e—Adaxial epidermis,outer surface;f—Abaxial epidermis,outer surface.Arrow 1—A cell,anticlinal walls undulated;Arrow 2—A cell,slightly concave,having a pit on the periclinal wall;Arrow 3—An epidermal hair;Arrow 4—A salt gland,sunken;Arrow 5—A cell,surface swollen.

4.3. Key to the species of the genus Tamarix from China

Table 3 Foliar, floral and fruit characters of Tamarix species from China(Liu et al.,2012;Yang and Gaskin,2007).

Thus,based on our studies,the features of flowers in combination with the leaf epidermal characters show clear taxonomical differentiation.New taxonomical evidence shows the occurrence of 13 species and four variants of the genus Tamarix in China.

4.4. Systematic implication

Although the plants of Tamarix from China are mainly distributed in cool,arid or semi-arid areas,their ancestors from the coastal areas of the ancient Mediterranean Sea probably lived in warm and humid climates during the Eocene(Zhang et al.,2003a).Papillae or epidermal hairs,which are outgrowths of the outer epidermal cells and facilitate leaves to respond to the water stress,are commonly seen in plants growing in arid or semi-arid areas in contrast to plants growing in warm and humid climates(Evert,2006;Ferris et al.,1996;Glover,2010).In Tamarix,they are of relatively recent origin.Thus,primitive species lack or have fewer papillae or epidermal hairs,while the more evolved species likely possess these structures abundantly.

Of the species with a five-merous flower,T.taklamakanensis lacks papillae or epidermal hairs on both adaxial and abaxial epidermis(Fig.1w and x),and would be the most primitive one;while T.hispida has the leaf covered with long epidermal hairs on both the adaxial and abaxial epidermis(Fig.3k and l),and would be the most evolved species.T.albiflonum and T.austromongolica have papillae on the adaxial epidermis(Fig.2e and 2k),while the abaxial epidermis lacks papillae or epidermal hairs(Fig.2f and l).They are likely to be more evolved than T.taklamakanensis(Table 4).In T.chinensis,T.leptostachya and T.karelinii,the papillae occur on both adaxial and abaxial epidermis(Figs.2q,r,w,x and 3e,f),so they are more evolved than T.albiflonum and T.austromongolica(Table 4).T.ramosissima is considered to be highly evolved compared to the above three species,because their papillae on the adaxial epidermis have elongated(Table 4;Fig.3q).

Similarly,in the species with a four-merous flower,T.elongata and T.laxa would be more evolved than T.androssowii according to the distinct and stout papillae on the adaxial epidermis(Table 4;Fig.1e and k),since the papillae in T.androssowii are slender and small(Fig.1q).

As discussed above,the epidermal characters of T.gracilis and T.gansuensis are intermediate between species with a four-merous flower and those with a five-merous flower.T.gracilis has stout and ballshaped papillae on the adaxial epidermis,but its abaxial epidermis is flat(Fig.4w and x);while T.gansuensis bears obvious epidermal hairs or papillae on both the adaxial and abaxial epidermis(Fig.5e and f).Accordingly,T.gansuensis seems to be the more evolved species(Table 4).

4.5. Phylogenetic relationships between species of Tamarix from China

Based on previous studies(e.g.,Baum,1978;Zhang et al.,2003a),the species of Tamarix which have only four-merous flowers are more evolved than those which have only five-merous flowers,and the species which have both four-merous and five-merous flowers are considered to be transitional types from the fivemerous to the four-merous stage.In order to gain a clear understanding of the phylogenetic relationships of the species in China,a cladistic analysis based on the epidermal characters(Tables 5 and 6)for the 13 species of the genus has been performed using SPSS 17.0(Fig.6).

4.6. Ecological and palaeogeographic implications

As a typical old-world temperate genus,the present distribution of Tamarix is discontinuous,mainly in the arid and semiarid regions around the coast of the ancient Mediterranean Sea and in the central Asia;some of the species are also found in the southwestern Africa,southern India and eastern Asia.Thus,although the earliest fossils of the genus were considered tostem from the early Oligocene of Egypt(Tamaricoxylon africanum(Kr¨ausel)Boureau)(Baum et al.,1970;Monique and Jean,1995),according to the palaeogeographic pattern and the primitive characters of the group in India,the ancestors of the genus Tamarix are thought to have originated in the Eocene of the Tethys area and lived in warm and humid environments(Li et al.,2012;Zhang et al.,2003a).

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Table 4 Systematic implication of Chinese Tamarix based on leaf epidermal characters.

Flower merous Abaxial epidermis Adaxial epidermis Additional Tamarix species Distribution characters 5 Papillae absent Papillae absent No T.taklamakanensis Xinjiang,Gansu(China)Papillae absent Papillae conspicuous,stout No T.albiflonum Xinjiang(China)Papillae absent Papillae conspicuous,hair-like No T.austromongolica Qinghai,Gansu, Ningxia,Inner Mongolia,Shannxi,Shanxi,Hebei,Henan,Shandong (China)Papillae inconspicuous Papillae conspicuous,stout No T.karelinii Xinjiang,Qinghai, Gansu,Inner Mongolia(China);Afghanistan,Mongolia,Russia,Southwest Asia Papillae conspicuous Papillae conspicuous,stout Cells polygonal onT.chinensis Liaoning,Hebei,Henan,Shandong,Jiangsu,abaxial epidermisAnhui(China)Papillae conspicuous Papillae conspicuous,stout Cells spindle-shapedT.leptostachya Xinjiang,Qinghai,Gansu,Ningxia,Inner on abaxial epidermis Mongolia(China);Mongolia,Central Asia Papillae conspicuous Epidermal hairs conspicuous No T.ramosissima Xinjiang,Qinghai,Gansu,Ningxia,Inner Mongolia(China);Afghanistan,Mongolia,Central—Southwest Asia,East Europe Epidermal hairs conspicuous Epidermal hairs conspicuous No T.hispida Xinjiang,Qinghai,Gansu,Ningxia,Inner Mongolia(China);Afghanistan, Mongolia,Central—Southwest Asia 4 and 5 Papillae absent Papillae conspicuous No T.gracilis Xinjiang,Qinghai,Gansu,Inner Mongolia(China);Kazakhstan, Mongolia, Russia,Tajikistan,Turkmenistan,Southwest Asia Papillae present Epidermal hairs conspicuous No T.gansuensis Xinjiang,Qinghai,Gansu,Inner Mongolia(China)4 Papillae absent Papillae inconspicuous No T.androssowii Xinjiang,Gansu,Ningxia,Inner Mongolia(China);Mongolia,Central Asia Papillae absent Papillae conspicuous No T.laxa Xinjiang,Qinghai,Gansu,Ningxia,Inner Mongolia,Shannxi(China);Afghanistan,Kazakhstan,Mongolia,Russia,Turkmenistan,Southwest Asia Papillae absent Papillae conspicuous No T.elongata Xinjiang,Qinghai,Gansu,Ningxia,Inner Mongolia(China);Kazakhstan,Mongolia, Russia,Turkmenistan,Uzbekistan

Table 5 Characters and character states of Chinese Tamarix species.

Table 6 Data matrix for character states of Chinese Tamarix species.

In China,fossils of Tamarix are scarce.Spores from the Tertiary of Gansu Province were thought to be the earliest records(Jiang and Yang,1980;Sung,1958),but the taxonomic position of these fossils was doubted because of the morphological similarities to the Salicaceae (Zhang et al.,2003a).Based on phytogeographical studies,the first appearance of the genus Tamarix in China was at least in the late Miocene,accompanied by the uplift of the Qinghai—Tibet Plateau and the disappearance of the Tethys(Zhang et al.,2003a).Thus,the abundant papillae or epidermal hairs in leaves of the Chinese species were probably of relatively recent origin,and were acquired as adaptation to the arid or semi-arid environments in the Late Cenozoic of northwestern China.

These ecological adaptations of the epidermal features made it easy to speculate that the density of papillae or the length of epidermal hairs in Tamarix species are closely related to the environments in which they live.Species with lower papilla density or shorter epidermal hairs are found to be living in more humid and warmer climates,while species with greater papilla density or longer epidermal hairs are found to be living in more arid and harder climatic conditions.Our conclusions are consistent with the study of Li et al.(2007),in which they inferred that from its leaf epidermal features the Japanese honeysuckle has a stronger drought-resistance and uses water more efficiently than the wild honeysuckle,because the Japanese honeysuckle has more epidermal hairs on the lower epidermis,which could form a relatively air proof space and reduce water loss from stomata under severe water deficit conditions.The lower epidermis of the Japanese honeysuckle is an efficient water trap.

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Ecological or palaeogeographic features of Tamarix in the Late Cenozoic of Northwest China can thus be determined on the basis of abundance of papillae or length of epidermal hairs on the surface of leaves.Among the species of Tamarix in China,T.taklamakanensis,which is now distributed in the Tarim Basin(Taklamakan desert and Kumtag desert)of Xinjiang and the Dunhuang City of Gansu(Liu et al.,2012;Yang and Gaskin,2007;Table 4),lackspapillae or epidermal hairs on both the adaxial and abaxial epidermis;while T.hispida,which is distributed in the desert areas of Xinjiang,Qinghai,Gansu,Ningxia and Inner Mongolia(Liu et al.,2012;Yang and Gaskin,2007;Table 4),has long epidermal hairs on both the adaxial and abaxial epidermis.We infer that the palaeoecological or palaeogeographic conditions in the Late Neocene of the Tarim Basin and Dunhuang,where T.taklamakanensis is now found,were characterized by a predominantly warmer and more humid climate than the areas where T.hispida are found.

寿司最傻了,比我傻多了!有一次它在玩跑轮,跑得贼快贼快,过了一会儿,可能是累了,忽然停了下来。它不知道有惯性,一下被甩了出来,前脚和后脚在空中动来动去,叭的一声摔在地上,成了一块饼!我在那里笑,没想到我傻,它比我更傻!我以为它在跑轮里面吃了亏,会怕这个跑轮,不敢再上去了。没想到,它直接跑到跑轮上面上厕所,上完还在上面跑。傻是不是我们俩的亮点?就在我想这个问题的时候,鹩哥的饭没了,乌龟被太阳烤着,水被晒得滚烫滚烫的……

Fig.6 Dendrogram of Chinese Tamarix species based on epidermal characters.

Acknowledgements

This research was supported by the National Natural Science Foundation of China,Grant 41271070 and the West Light Foundation of the Chinese Academy of Sciences,Grant 2015-XBQN-B-25.The authors thank Prof.Kai-Yun Guan for the coordination of plant collections,Dr.Ya Li and Dr.Mei-Lin Yang for providing some references,Dr.Ru Feng for technical help,and the Lab Center of Xinjiang Institute of Ecology and Geography,Chinese Academy of Sciences,for preparing the experiments.

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Jian-WeiZhang,AshalataDRozario,Shi-MinDuan,Xi-YongWang,Xiao-QingLiang,Bo-RongPan
《Journal of Palaeogeography》2018年第2期文献

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