Research Journal of Agriculture and Biological Sciences, 4(6): 725-733, 2008 © 2008, INSInet Publication

The Morphological and Anatomical Properties of argentea L. () in Turkey

Pelin Baran, Cânan Özdemir and Kâmuran Aktaş

Celal Bayar University, Faculty of Art and Science, Department of Biology, Manisa/Turkey.

Abstract: In this study, the morphological and anatomical properties of Salvia argentea L. (Lamiaceae) have been investigated. S. argentea has a perennial taproot. The stem is erect and quadrangular. Leaves are simple. Inflorescense is verticillate cyme. The upper lip of corolla is white, tinged light lilac at the top. The lower lip is cream. In our research, the cross-sections of root, stem, leaf, petiole, calyx and corolla are indicated. The anatomical features are discussed. Results are presented with photographs, drawings and tables.

Key words: Anatomy, Lamiaceae, Morphology, Salvia, Salvia argentea, Turkey

INTRODUCTION and anatomical characters, except a few species[6,17,7,20,21,5,19,2]. Any morphological and anatomical Many species of Lamiaceae are aromatic and often study in detail, has not been found in the literature, used as herbs, spices, folk medicines, and a source of except the main morphological knowledge of S. fragrance[25]. Salvia, the largest genus of the family argentea in “Flora of Turkey”[15]. In this study, we Lamiaceae, represents an enormous and cosmopolitan aimed to introduce morphological and anatomical assemblage of nearly 1000 species displaying a characters of Salvia argentea in detail. remarkable range of variation. The genus comprises 500 spp. in Central and South America, 250 spp. in MATERIALS AND METHODS Central Asia/Mediterranean, and 90 spp. in Eastern Asia[24]. Turkey is a major diversity centre for Salvia in samples were collected from natural Asia[23]. Since the most recent works of the genus in populations between 2003-2004. Some samples were Turkey, four new species have been described; the total used for morphological and anatomical studies, some has now reached 90. 47 of these Salvia species in were dried as herbarium sample. Samples were Turkey are endemic[15,8,11,10,14]. collected from the following locations: Salvia species are important group of useful which have not lose their importance since ancient CB1 İzmir: Kemalpaşa Nif mountain, roadside, c. times. The genus is named “Salvia” derived from 1500 m, 15.vi.2003, Baran 015 “Salveo” which means “to save, to recover” in Latin[13]. CB1 Manisa: Spill mountain, rocky place, c.1500 m, Salvia, commonly known as sage, has multiple uses 20.vi.2004, Baran 016 such as condiment, food additive, seasoning, spice and herbal tea[9]. The seeds of Salvia species often produce The taxonomical description of the species follows mucilage on wetting[15]. This clear mucilage that the Hedge[15]. Anatomical studies were carried out on the seeds give off on wetting is used for lacquerware and samples kept in alcohol 70%. The paraffin method was is mixed with fruit juices to produce pleasant drinks[12]. applied for preparing the cross-sections of root, stem, In the East countries, that mucilage is used for the leave, petiole and flower using microtome[1]. treatment of eye diseases[3]. Beside Salvia species have medicinal value, they are also grown in parks and RESULTS AND DISCUSSION gardens as ornamental plants[18]. Historically, Salvia argentea leaves have been used against wounds, Results: probably as a haemostatic. The appearance of the Morphological Properties: Perennial root with a thick, young leaves, which are very hairy, may have played dark brown outer cover was taproot. Stem was erect, a role in the folk ‘perception’ of the external medical clearly quadrangular. Stem branchs were arranged properties of the species[22]. Most of Salvia species decussately. Stem indumentum was pilose. Leaves, have not been investigated in point of morphological differing between ovat and oblong were simple, mostly

Corresponding Author: Pelin Baran, Celal Bayar University, Faculty of Art and Science, Department of Biology, Manisa/Turkey. Tel: +905325584663 Fax: +902362412158 E-mail: [email protected], [email protected] 725 Res. J. Agric. & Biol. Sci., 4(6): 725-733, 2008 basal. Leaf edge was irregularly erose. Leaf epidermis cells were sinuous walled (Fig. 3 C-F, indumentum was villose. Leaf venation was reticulate- Table II). pinnate. Petiole indumentum was villose. was verticillate-cyme. Flowers were zigomorphic, Petiole: Epidermis, the outermost layer, was formed by located at the base of bracts. Flowers were 2-4, 6 in cells oval, squarish or nearly rectangular. Parenchyma a verticel. The upper lip of calyx was tridentate and with circular cells and intercellular spaces was 17-23 the lower lip was bidentate. Calyx indumentum layered under epidermis. Discontinous collenchyma was was villose. The upper lip of bilabiate corolla was present under epidermis. collateral vascular bundles white, tinged light lilac, strongly falcate, compressed were 5 or 7 and large in the center and 3-5 and small from laterals, two small lobed at the end and the in the ends of the petiole. The central vascular bundles lower lip was cream. The median lobe of three lobed had 49-69 xylem rays (Fig. 4 A-C, Table II). lower lip was the largest one and two small lobed at the end. Corolla tube was ventricose. Stigma was Calyx: Adaxial and abaxial epidermis were single unequally bifurcated. Stamens were B type. Fruit of layered and with diacytic stomata. Cuticle was the four dry nutlets were light brown, trigonous, thickest where the large vascular bundles were present. mucilaginous on wetting. Seed surface was reticulate The outer surface of epidermis cells was sinuous patterned. Bracts were acuminate. The plant were walled and without papilla. Abaxial epidermis cells densely covered with glandular and eglandular hairs were usually larger than those adaxial. Parenchyma (Fig .1, Table I). with a lot of chloroplasts and intercellular spaces was 4-7 layered (Fig. 4 D-F, Table II). Anatomical Properties: Root: Peridermis was 5-6 layered at the outermost of Corolla: The outer surfaces of epidermis cells were the cross-section. Parenchymatous cortex under sinuous walled and sometimes with papilla or smooth. peridermis was 4-7 layered in young root and 18-20 A thin cuticle surrounded epidermis cells. Epidermis layered in old root. Sclerenchyma groups were present cells were larger at where vascular bundles were both on phloem and at primary cortex in old root. present. Parenchyma with large intercellular spaces was Cambium was unclear. Trachea cells were gradually 1-2 layered (Fig. 4 G-J, Table II). enlarged towards the outer. Center of young root was filled with xylem, in contrast to that of old root filled Discussion: Our morphological findings of S. argentea with parenchymatous pith. Pith rays were 1-32 rowed are comparable with the description of the taxon in (Fig. 2, Table II). “Flora of Turkey”[15] except for the qualitative properties of morphology, taking into consideration that Stem: Stem was clearly quadrangular in the cross- our findings belong to the period of 2003-2004. section. Epidermis, single layered, was formed by oval, The difference in the number of the collected plant squarish or nearly rectangular cells. 2-12 layered samples in “Flora of Turkey” and also the changes in collenchyma was present only at the corners of stem. the climatical conditions for years may be responsible Cortex, formed by parenchymatous, circular and oval for some differences in our numerical data. On the cells was 12-19 layered at the edges and 5-11 layered other hand, morphological measurements of the anther, at the corners. Cortex cells near epidermis was smaller filament and pistil of the examined species have been than those near vascular bundles. Sclerenchyma groups firstly reported in this study. Salvia is separated from were present on the vascular bundles. Phloem was other members of the family on the basis of its unusual located under sclerenchyma. 1-2 layered cambium not staminal structure. Staminal morphology is the major very clear was located between phloem and xylem. defining character of the genus, which is often Xylem part was larger than phloem part. Vascular associated with an unusual pollination syndrome in bundles at the corners were larger than those at the which the pollinator pushes against the posterior anther edges. A parenchymatous large pith was present at the thecae while accessing a nectar reward at the base of center of stem. Pith rays were 1-13 rowed (Fig. 3 A-B, the corolla tube, causing the anterior thecae to deposite Table II). pollen on the pollinator via a lever-like mechanism[24]. Stamens of S. argentea are recognised as type B. Leaf: Epidermis, formed by oval, squarish or nearly Staminal connectives are clearly longer than filaments. rectangular cells was single layered on the adaxial and The lower theca is reduced to a variously shaped abaxial surface. Leaf was bifacial consisting of a 1-3 sterile tissue that is usually dolabriform plate[15]. layered palisade parenchyma and a scattered spongy According to our observations, the corolla and stamen parenchyma. Diacytic stomata were present on both structure of S. argentea are well models explaining this adaxial and abaxial epidermis. Angular collenchyma mechanism, because its upper lip of corolla, that is surrounds the median vein. In the superficial sections, strongly falcate, facilitates the enter of insect to the

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Table I: Morphological measurements of plant organs of Salvia argentea L. Min. - Max. (cm) Mean ± S.D.* (cm) Root Root length 15 - 55 29.3 ± 15.3 ------Stem Stem length 20 - 56 42.5 ± 10.8 ------Leaf Leaf length 2 - 19.5 8.2 ± 3.9 ------Leaf width 1 -12 4.6 ± 2.5 ------Petiole Petiole length 0.8 - 9.5 3.7 ± 2.5 ------Flower Pedicel length 0.3 - 0.6 0.42 ± 0.08 ------Calyx length 0.8 - 1.7 1.14 ± 0.22 ------Length of calyx teeth 0.02 - 0.5 0.27 ± 0.14 ------Corolla length 1.7 - 3 2.29 ± 0.4 ------Filament length 0.4 - 0.6 0.49 ± 0.05 ------Anther length 0.4 - 0.5 0.41 ± 0.03 ------Pistil length 4 - 4.6 4.28 ± 0.2 ------Bract Bract length 0.6 - 1.8 1.08 ± 0.32 ------Bract width 0.6 - 1.5 1.06 ± 0.22 ------Seed Seed length 0.3 - 0.4 0.35 ± 0.05 ------Seed width 0.22 - 0.4 0.29 ± 0.05 *S.D. : Standart Deviation

Table II: Anatomical measurements of various tissue of Salvia argentea L. Width (µm) Length (µm) ------Min. - Max. Mean ± S.D.* Min. - Max. Mean ± S.D.* Root Peridermis cell 10.6 - 63.5 35.4 ± 18.4 5.3 - 42.4 21.6 ± 13.4 ------Parenchyma cell 5.3 - 26.5 17.5 ± 6.4 5.3 - 15.9 11.2 ± 3.6 ------Pith ray 10.7 - 214.3 112.5 ± 39.6 ------Trachea cell 5.3 - 39.7 23.2 ± 12.8 ------Pith cell 10.9 - 70.9 38.4 ± 26.2 Stem Epidermis cell 7.9 - 42.4 23.3 ± 10.7 10.6 - 47.6 27.9 ± 11.9 ------Parenchyma 5.3 - 79.4 30.2 ± 23.5 10.6 - 79.4 42.1 ± 21.9 ------Pith ray 7.9 - 375 99.8 ± 94 ------Trachea cell 5.3 - 52.9 26.8 ± 19.9 ------Pith cell 7.9 - 190.6 71.5 ± 60.9 Leaf Cuticle 2.7 - 13.2 8.5 ± 2.6 ------Adaxial epidermis cell 5.3 - 63.5 29.1 ± 19.2 7.9 - 37.1 24.1 ± 8.1 ------Abaxial epidermis cell 5.3 - 58.2 21.8 ± 16.7 5.3 - 37.1 19.4 ± 10 ------Mezophyll region 68.8 - 137.7 110.9 ± 22.8 ------

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Table 2: Continued Palisade region 21.2 - 55.6 39.4 ± 11.5 ------Spongy region 21.2 - 54.5 39.1 ± 10.2 ------Palisade cell 10.6 - 21.2 16.2 ± 4.1 29.1 - 50.3 36.2 ± 6.6 ------Spongy cell 5.3 - 42.4 23.2 ± 11.1 Petiole Adaxial epidermis cell 10.6 - 47.6 24.2 ± 13.6 7.9 - 39.7 20.8 ± 9.7 ------Abaxial epidermis cell 7.9 - 39.7 21.8 ± 11 7.9 - 39.7 22.8 ± 11 Diameter of cortex cell 5.3 - 142.9 65.1 ± 56 ------Trachea cell 5.3 - 47.6 25.4 ± 15.3 Bract Adaxial epidermis cell 10.6 - 60.9 36.7 ± 20.6 15.9 - 47.6 32.2 ± 11.7 ------Abaxial epidermis cell 10.6 - 76.8 37.6 ± 31.3 15.9 - 52.9 30.7 ± 18.1 ------Parenchyma cell 10.6 - 26.5 20.4 ± 6 15.9 - 47.6 29.4 ± 11.4 Calyx Adaxial epidermis cell 5.3 - 58.2 28.2 ± 16.3 7.9 - 47.6 21.6 ± 11.2 ------Abaxial epidermis cell 5.3 - 63.5 32.6 ± 18.9 5.3 - 63.5 28.5 ± 16.7 ------Parenchyma cell 10.6 - 31.8 21.2 ± 5.8 10.6 - 42.4 25.5 ± 9.7 Trachea cell 2.7 - 21.2 13.8 ± 6.9 Corolla ------Adaxial epidermis cell 23.8 - 63.5 34 ± 11.2 23.8 - 52.9 37.5 ± 9.8 ------Abaxial epidermis cell 10.6 - 58.2 30.3 ± 13.9 15.9 - 79.4 34.8 ± 18.8 ------Parenchyma cell 10.6 - 68.8 39.4 ± 19.6 10.6 - 42.4 22.5 ± 9.2 Trachea cell 2.7 - 7.9 5.3 ± 2.1 *S.D. : Standart Deviation tube besides the median lobe of the lower lip, that is numbers of pith rays in the roots show variation concave and largest, provides insects a convenient between 1-10 for S. palaestina[6], 1-3 for S. landing platform, in addition to the stamens type B. trichoclada[7], 1-8 for S. sclarea[20], 2-40 for S. We compared our anatomical findings of S. forskahlei[20], 2-6 for S. napifolia[2]. Row number of the argentea with the anatomical studies made on other pith rays might be used as a species-distinguishing Salvia species in literature. Some researchers reported feature, because it differs in each species. The root the presence of schlerenchyma groups in the cortex center is filled with primery xylem in S. palaestina, S. region of the roots and stems of S. palaestina, S. trichoclada, S. sclarea, S. napifolia[6,7,20,2] while that of trichoclada, S. napifolia[6,7,2] while Özdemir and S. forskahlei has a large pith region[21]. We observed a Şenel[21] mentioned an additional sclerenchymatous ring large pith consisting of parenchymatous cells in the surrrounding the sclerenchyma groups in the root root center of S. argentea and pith rays 1-32 rowed. cortex, which is being alone in the herbaceous stem of The characteristic feature of Lamiaceae family is S. forskahlei. We observed clear sclerenchyma groups a quadrangular stem and a well-developed upon the phloem and additionally within the cortex collenchyma, supporting tissue at the corners of parenchyma but no sclerenchymatic ring in the root and stem[16]. The discontinous angular collenchyma at the stem of S. argentea. corners of the quadrangular stems of S. pallida Vacular cambium is reported as 2-3 layered in the Bentham and S. procurrens Benth. is reported. İt is stems of S. palaestina and S. forskahlei[6,21] or 3-4 layered in the petiole of S. pallida while it is sometimes unclear as seen in the stems of S. sclarea 1-2 layered at the dorsal and lateral parts, 3-4 and S. napifolia[20,2]. We observed a 1-2 layered layered at the lobes of the petiole of S. procurrens[19]. vascular cambium in the stem of S. argentea. In correspondance with the other references[6,7,20,21,2], Pith rays of Lamiaceae family are 2-12 or more a well-developed collenchyma has been seen at the rowed and quite heterogeneous in structure[16]. Rays in corners of the quadrangular stem of S. argentea. A few the wood of S. pubescens, S. regla, S. sessei are layered discontinous collenchyma has also been seen reported as heterogeneous in the literature[5]. The row here and there in the petiole.

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Fig. 1: General appearence and some parts of Salvia argentea L. A-B.General Appearence, C.Corolla, D.Calyx, E.Seed, F.Bract, G.Stamens, H.Pistil

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Fig. 2: The root section of Salvia argentea L. pe: peridermis ph: phloem t: trachea cp: cortex parenchyma ca: cambium pr: pith ray s: sclerenchyma x: xylem p: pith

The structure of vascular bundles in the cross- petiole. Our finding correspondes with that of section of petiole in Lamiaceae species may be Nakipoğlu and Oğuz[17], in point of the central vascular important in point of [16]. Nakipoğlu and bundle of the petiole, being divided into various Oğuz[17], who studied 7 Salvia species, separated number of pieces. vascular bundles of the petioles into two groups as Leaf mesophyll of Salvia species is entirely those in the species with basal leaves and those in the parenchymatous and the median vein of leaf is species without basal leaves. According to this surrounded by collenchyma[16]. The mesophyll of separation, the central vascular bundle of Salvia species S. sclarea, S. forskahlei, S. pallida, S. procurrens, with basal leaves is divided into pieces, while that S. napifolia[20,21,19,2] is bifacial while it is isobilateral without basal leaves is single, large and undivided[17]. for S. palaestina[6] and uniform for S. trichoclada[7]. Although S. napifolia is a plant with basal leaves, the S. trichoclada, S. sclarea, S. pallida, S. procurrens, S. central vascular bundle of petiole shows variation, napifolia have subepidermal angular or angular- being sometimes divided into 2-3 pieces or on the lacunar collenchyma at the region of median contrary sometimes single, large and lobed[2]. S. vein[7,20,19,2] . The mesophyll of S. argentea was argentea, a plant with basal leaves, had 4-7 central bifacial having lacunar collenchyma surrounding the vascular bundles and 3-5 small bundles at each end of median vein.

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Fig. 3: The stem and leaf sections of Salvia argentea L. A-B. Stem, C-D. Leaf, E. Adaxial epidermis of leaf, F. Abaxial epidermis of leaf e: epidermis cp: cortex parenchyma ca: cambium p: pith ph: phloem gh: glandular hair s: sclerenchyma x: xylem cu: cuticle t: trachea st: stoma co: collenchyma eh: eglandular hair ad: adaxial epidermis v: vascular bundle pp: palisade parenchyma sp: spongy parenchyma ab: abaxial epidermis

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Fig. 4: The petiole and flower sections of Salvia argentea L. A-C. Petiole sections, D-F. Calyx sections G-J. Corolla sections e: epidermis ad: adaxial epidermis ab: abaxial epidermis cu: cuticle pl: papilla pa: parenchyma v: vascular bundle gh: glandular hair eh: eglandular hair

The calyx and corolla of S. argentea were densely In conclusion, we aimed to introduce morphological covered with glandular hairs. Epidermis cells of the and anatomical properties of S. argentea, a perennial corolla had sometimes papilla on their outer surfaces as plant, in detail in this paper. We found some reported in S. napifolia[2]. differences beside the similarities between S. argentea

732 Res. J. Agric. & Biol. Sci., 4(6): 725-733, 2008 and the other Salvia species in literarature. S. argentea 12. Estilai, A., A. Hashemi and K. Truman, 1990. was densely covered with glandular hairs which Chromosome number and meiotic behavior of abundantly produce sticky substances and volatile oil. cultivated chia, Salvia hispanica (Lamiaceae). We suggest that S. argentea may be important in Hortscience 25: 1646-1647. medicine and economy because of its abundant 13. Hamlyn, P., 1969. The Marshall Cavendish, secretory substances. In addition, S. argentea with Encyclopedia of Gardening Vol. 19, Garrod and large, white and violet tinged flowers and the leaves Lofthouse International, London forming a rosette at the base can be also used as an 14. Hamzaoğlu, E., A. Duran and N.M. Pınar, 2005. ornamental plant in park and gardens. Salvia anatolica (Lamiaceae), A new species from East Anatolia, Turkey. Ann. Bot. Fennici 42: REFERENCES 215-220. 15. Hedge, I.C., 1982. Salvia L. In: Davis PH (ed.) 1. Algan, G., 1981. Bitkisel dokular için mikroteknik, Flora of Turkey and The East Aegean Islands, Fırat Üniv. Fen-Ed. Fak. Yayın. Bot. No: 1, 7: 400-461. Edinburgh: Edinburgh Univ. Press. İstanbul. 16. Metcalfe, J.R. and L. Chalk, 1972. Anatomy of 2. Baran, P. and C. Özdemir, 2006. The the Dicotyledons. Vols. 2, Oxford: Clarendon morphological and anatomical characters of Salvia Press. napifolia Jacq. in Turkey. Bangladesh J. Bot. 35: 17. Nakipoğlu, M. and G. Oğuz, 1990. İzmir 77-84. çevresinde yayılış gösteren bazı Salvia (adaçayı) 3. Baytop, T., 1999. Türkiye’de bitkilerle tedavi türlerinin biyosistematiği üzerine araştırmalar. (geçmişte ve bugün). 2. Baskı, Nobel Tıp E. Ü. Fen Bil. Enst. Derg., 1: 23-29. Kitapevleri, Çapa-İstanbul, Konak-İzmir, Sıhhıye- 18. Nakipoğlu, M., 1993. Bazı adaçayı (Salvia L.) Ankara, pp: 142-144. türleri ve bu türlerin ekonomik önemi. Dokuz Eylül 4. Bisio, A., A. Corallo, P. Gastaldo, G. Romussi, G. Üniversitesi Yayınları, Eğitim Fakültesi, Eğitim Ciarallo, N. Fontana, N. De Tommasi and P. Bilimleri Dergisi 6: 45-58. Profumo, 1999. Glandular hairs and secreted 19. Novoa, M.C., C. Monti and C.E. Vizcaino, 2005. material in Salvia blepharophylla Brandegee ex Anatomia y etnobotanica de cuatro especies de Epling Grown in Italy. Annals of Botany 83: Labiateae de la provincia biogeografica pampeana, 441-452. usadas en la medicina popular. Acta Farm. 5. Ceja-Romeo, J., C.P. Perez-Olvera and J. Rivera- Bonaerense, 24: 512-520. Tapia, 2005. Anatomia de la madera de las 20. Özdemir, C. and G. Şenel, 1999. The especies Mexicanas de Salvia seccion morphological, anatomical and karyological Erythrostachys Epl. (Lamiaceae). Bol. Soc. Bot. properties of Salvia sclarea L. Tr. J. Bot. 23: Mex. 76: 53-59. 7-18. 6. Çobanoğlu, D., 1988. Salvia palaesthina 21. Özdemir, C. and G. Şenel, 2001. The Bentham’ın (Lamiaceae) morfolojik ve sitolojik morphological, anatomical and karyological özellikleri. Doğa Bilim Dergisi: Biyoloji 12: properties of Salvia forskahlei L. (Lamiaceae) in 215-223. Turkey. J. Econ. Taxon. Bot., 19: 297-313. 7. Çobanoğlu, D., S. Özel and H. Evren, 1992. 22. Pieroni, A., C.L. Quave and R.F. Santoro, 2004. Salvia trichoclada Bentham (Lamiaceae)’nin Folk pharmaceutical knowledge in the territory of morfolojik özelikleri. XI. Ulusal Biyoloji Kongresi, the Dolomiti Lucane, inland southern Italy. Journal Elazığ, 24-27 Haziran, Botanik, 83-89. of Ethnopharmacology, 95: 373-384. 8. Davis. P.H., R.R. Mill and K. Tan, 1988. Flora of 23. Vural, A. and N. Adıgüzel, 1996. A new species Turkey and The East Aegean Islands (Suppl.), from Central Anatolia: Salvia aytachii M. Vural et Vol. 10, Edinburgh: Edinburgh Univ. Press. N. Adıgüzel (Labiatae). Tr. J. Bot., 20: 531-534. 9. Demirci, B., F. Demirci, A.A. Dönmez, G. Franz, 24. Walker, J.B., K.J. Sytsma, J. Treutlein and M. D.H. Paper and K.H.C. Başer, 2005. Effects of Wink, 2004. Salvia (Lamiaceae) is not Salvia essential oils on the chorioallantoic monophyletic: Implications for the systematics, membrane (CAM) assay. Pharmaceutical Biology, radiation, and ecological specialization of Salvia 43: 666-671. and Tribe Menthae. American Journal of Botany 10. Dönmez, A.A., 2001. A new Turkish species of 91: 1115-1125. Salvia L. (Lamiaceae). Botanical Journal of 25. Werker, E., U. Ravid and E. Putievsky, 1985. Linnean Society, 137: 413-416. Structure of glandular hairs and ıdentification of 11. Duman, H., 2000. Salvia L. In: Güner, A., N. the main components of their secreted material in Özhatay, T. Ekim and K.H.C. Başer, (eds.) Flora some species of the Labiatae. Israel Journal of of Turkey and The East Aegean Islands. Vol. 11, Botany 34: 31-45. Edinburg: Edinburg University Press.

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