Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2003? 2003 1433 323330 Original Article HAIRS IN THORNY ASTRALAGUS SPECIES S. ZARRE Botanical Journal of the Linnean Society, 2003, 143, 323–330. With 26 figures Hair micromorphology and its phylogenetic application in thorny species of Astragalus (Fabaceae) SHAHIN ZARRE* Department of Biology, Faculty of Science, University of Tehran, PO Box 14155–6455, Tehran, Iran A comprehensive survey and descriptions of hair characters in thorny species of Astragalus have been conducted using light and scanning electron microscopy. Attention was paid to hair colour, length, shape and papillae on the hair surface. On the basis of already defined phylogenetic relationships among the species in this group, apomorphic and plesiomorphic states are suggested for hair characters. The presence of black hairs in the region of inflorescence, papillae on the hair surface and flattened ribbon-like hairs are the most important plesiomorphies. Moreover, there is a tendency to have long hairs in several advanced groups. Astragalus sect. Acanthophace, A. sect. Adiaspastus, A. sect. Aegacantha, A. sect. Anthylloidei and A. sect. Stipitella present the most primitive hair types in the thorny group. These sections have also been previously established as primitive with respect to several other morphological characters such as pod structure and the shape of the standard. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330. ADDITIONAL KEYWORDS: flattened hairs – hair colour – hair length – phylogeny – subgeneric classification – subtribe Coluteinae. INTRODUCTION The importance of hair characters in the systematics of Astragalus was recognized when Bunge (1868– 1869) presented his inclusive classification system for the genus. According to him two subgenera, Cercidothrix and Calycocystis, were characterized by having medifixed hairs. Among the eight subgenera recognized for Astragalus by Bunge, only two were accepted by Podlech (1982), viz. A. subgen. Astragalus, characterized by basifixed hairs, and A. subgen. Cercidothrix, characterized by medifixed ones. Beside hair attachment, the overall shape of hairs and the inclusions on the hair surface were shown to be important in the phylogeny of Astragalus (Zarre, 2000). Hair characters were also used to transfer A. semnanensis Sirj. & Rech.f. from A. sect. Leucocercis (belongs to A. subgen. Cercidothrix) into a new monotypic section A. sect. Semnanenses (Zarre & Podlech, 2002). Moreover, the unique type of hairs in A. sect. Acanthophace were used in considering *E-mail: zarre@khayam.ut.ac.ir A. cryptocarpos DC. as a member of this section (Zarre & Podlech, 2001a). Detailed micromorphological studies on hairs in the different natural groups within thorny Astragalus (for terminology see Zarre, 2000), the subject of this paper, can lead to new aspects relating to systematics of Astragalus and clarify the ambiguities in the systematics of this group. MATERIAL AND METHODS This study is mainly based on observation and measurement of hair characters in all parts of several species belonging to thorny Astragalus. In several cases more than five specimens were analysed for one species to ensure certainty about the stability of hair characters among different specimens of one species. The herbarium material for this study is located in the Munich herbarium (M). A list of voucher specimens is available from the author upon request. Detailed examination of hair characters was carried out using a Willd–Heerbrugg dissecting microscope. Scanning electron microscopy was carried out to better observe the detailed structure of the hair surface in several © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 323 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 Received November 2002; accepted for publication June 2003 324 S. ZARRE species, using a Leo 962 instrument at the Institut für systematische Botanik der LMU, Munich (Germany). RESULTS Thorny species of A. subgen. Astragalus in the Old World may be placed in 15 sections Zarre (2000). The hairs in the thorny Astragalus group are always unicellular and basifixed. The medifixed hairy species of Astragalus, e.g. the species of A. sect. Leucocercis, were not considered in the analysis, because it had been established previously (Podlech, 1982) that they are not related to the thorny group. A short description of hair characters in each section is presented below. A. SECT. ACANTHOPHACE (FIGS 1–6) Except for A. sclerocladus Bunge with exclusively white hairs, the indumentum in the rest of this section 2 3 4 5 6 Figures 1–6. Leaf hairs in Astragalus sect. Acanthophace. Fig. 1. A. sclerocladus. Scale bar = 50 mm. Fig. 2. A. lycioides. Scale bar = 10 mm. Figs 3, 4. A. horridus. Scale bars = 20 and 10 mm respectively. Fig. 5. A. hezarensis. Scale bar = 100 mm. Fig. 6. A. ovigerus. Scale bar = 20 mm. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 1 HAIRS IN THORNY ASTRAGALUS SPECIES A. SECT. ADIASPASTUS (FIGS 7–10) Exclusively white hairy species are much more frequent in this section than those with mixed colours. In some species, e.g. A. brachycalyx Fisch., the longest hairs do not exceed 1.5 mm, whilst they are about 2.5– 4.5 mm in the rest of the section. The hairs are cylindrical-filiform, not or sparsely papillose and mostly striate on surface. Again appressed and spreading indumenta are present among different species of this section. For a detailed description on hair characters in this section see Zarre (2000). A. SECT. AEGACANTHA (FIGS 11,12) Although some species (e.g. A. altimurensis I. Deml and A. antheliophorus I. Deml) are exclusively white haired, most other species possess white and black hairs at least in the region of inflorescence. In most species the hairs are up to 2 mm long, but on the calyx they can reach 3.5 mm in a few species. The hairs are filiform in shape and papillose on the surface. Both spreading (more frequently) and appressed indumentum types can be found in this section. According to Deml (1972) this section is composed of 50 species, for each of which she presented an exact description of hair characters. A. SECT. ANTHYLLOIDEI (FIGS 13,14) Tietz & Zarre (1994) give a detailed taxonomic description of the species within this section and also describe hair characters for these species. In most species the hairs are white mixed with black in the region of inflorescence. Astragalus coluteopsis Parsa, A. ebenoides Boiss. and A. tortuosus DC. are some examples of exclusively white hairy species of this section. In A. flexilipes Bornm. and A. pseudotortuosus Tietz & Zarre the hairs are yellowish in colour. The hairs on the calyx are up to 1.5 mm long in some species and up to 4 mm in others. In a group of species, including e.g. A. noziensis Sirj. & Rech.f and A. lumsdenianus Aitch. & Baker, the hairs on leaves (Fig. 13) are cylindrical-canaliculate and papillose on the surface, but on the calyx (Fig. 14) the hairs are of two types: most hairs are relatively long (about 3 mm) and not papillose on the surface, and between these there are some short (about 0.6 mm) flattened ones, densely papillose on the surface. In A. diopogon Aitch. & Baker and A. szovitsii Fisch. & C. A. Mey. the hairs are sparsely or not papillose on the surface. Species with small and sparsely arranged papillae are very frequent in this section. A. SECT. CAMPYLANTHUS (FIG. 15) The hairs in this section are exclusively white. Long calyx teeth and hairs (up to 4 mm) beside campanulate calyx are characteristic for this section. The hairs in most species of this section are spreading, cylindrical and not papillose on the surface. For a detailed taxonomic description of the species in this section, see Tietz (1988). A. SECT. DIACME (FIG. 16) Astragalus roussaeanus Boiss. is the only member of this monotypic section and is exclusively white hairy. The hairs are spreading and up to 1.5 mm on leaves and up to 3 mm long on the calyx. These hairs are flattened and not or sparsely papillose on surface. A. SECT. ERIOSTOMA (FIG. 17) The low density of indumentum and shortness of the hairs (up to 1 mm) are characteristic for this monotypic section. Astragalus eriostomus Bornm. is covered by white hairs only. Interestingly, the surface of the calyx tube in this species is glabrous, but some hairs are present on the calyx teeth. The hairs in A. eriostomus are cylindrical-canaliculate and not papillose on the surface. A. SECT. HYMENOSTEGIS (FIG. 18) The hairs in this section are white only. Yellowish hairs are characteristic of A. hymenocystis Fisch. & C. A. Mey. and A. recognitus Fisch. & C. A. Mey. The length of hairs can reach 2.5 mm on rachides or peduncles and 4.5 (in most species) or 6 mm (in A. glumaceus Boiss. and A. kohrudicus Bunge) on the calyx. The hairs are again cylindrical-filiform and not papillose on the surface. For a detailed description of the species of this section, see Zarre & Podlech (1996). A. SECT. MACROPHYLLIUM (FIGS 19,20) In this recently revised section (Zarre, 2000), the hairs are exclusively white and very long (up to 6 mm on the © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 is composed of white and black hairs in the region of the inflorescence. The hairs are up to 0.8 mm long on vegetative parts and up to 1.5 mm on the calyx. They are in almost all parts of the plants flattened, ribbonlike and densely papillose on the surface. In most cases these hairs are strongly appressed to the surface of the bearing organs, but in some species, e.g. A. ovigerus Boiss. and A. lycioides Boiss., some ascending hairs can be distinguished on rachides and calyces (see Zarre & Podlech, 2001b). In A. ovigerus and A. hezarensis Zarre & Podlech, mixed with the above named characteristic hair type of this section, are some long spreading hairs, which are not or loosely papillose on the surface (Figs 5,6). 325 326 S. ZARRE 8 9 10 11 12 13 14 Figures 7–14. Leaf hairs in Astragalus sect. Adiaspastus. (Figs 7–10). A. sect. Aegacantha (Figs 11,12). A. sect. Anthylloidei (Fig. 13) and calyx hairs in A. sect. Anthylloidei (Fig. 14). Fig. 7. A. brachycalyx. Scale bar = 100 mm. Fig. 8. A. icmadophilus. Scale bar = 100 mm. Fig. 9. A. iodotropis. Scale bar = 200 mm. Fig.10. A. leiophyllus. Scale bar = 100 mm. Fig. 11. A. ajfreidii. Scale bar = 100 mm. Fig. 12. A. ajfreidii. Scale bar = 10 mm. Fig. 13. A. noziensis. Scale bar = 100 mm. Fig. 14. A. noziensis (calyx surface). Scale bar = 100 mm. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 7 HAIRS IN THORNY ASTRAGALUS SPECIES 16 17 18 19 20 21 22 Figures 15–22. Leaf hairs in Astragalus sect. Campylanthus (Fig. 15). A. sect. Diacme (Fig. 16). A. sect. Eriostoma (Fig. 17). A. sect. Hymenostegis (Fig. 18). A. sect. Macrophyllium (Figs 19,20). A. sect. Microphysa (Fig. 21), and A. sect. Polystegis (Fig. 22). Fig. 15. A. campylanthus. Scale bar = 100 mm. Fig. 16. A. roussaeanus. Scale bar = 100 mm. Fig. 17. A. eriostomus. Scale bar = 100 mm. Fig. 18. A. persicus. Scale bar = 200 mm. Fig. 19. A. dipodurus. Scale bar = 100 mm. Fig. 20. A. marashica. Scale bar = 100 mm. Fig. 21. A. ptycophyllus. Scale bar = 100 mm. Fig. 22. A. piptocephalus. Scale bar = 50 mm. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 15 327 328 S. ZARRE calyx). Contrary to an earlier suggestion for this section (Duman & Vural, 1990), no species is covered by glandular hairs (see Zarre & Duman, 1998). The leaves in most species of this section are glabrous or sparsely hairy. The only difference between the two closely related species A. oleaefolius DC. and A. dipodurus Bunge is that the leaf hairs are strongly appressed in the former and spreading in the latter. The hairs in this section are cylindrical-filiform and not papillose on surface. Exclusively white and short hairs (up to 2 mm long) are characteristic of this section. Because of its long calyx hairs and teeth in combination with an inflated fruiting calyx, A. argyrostachyus Boiss. is considered to be intermediate between this section and A. sect. Campylanthus (Tietz, 1988). The surface of hairs is ± sparsely papillose in this section and the hairs are again cylindrical-filiform. A. SECT. POLYSTEGIS (FIG. 22) The hairs are exclusively white, up to 2 mm long (on rachides) or 4 mm (on the calyx) and sparsely papillose in this monotypic section, which possesses the thickest bract texture among thorny Astragalus. A. SECT. POTERION (FIG. 23) A. SECT. SEMNANENSES (FIG. 25) A detailed description of hair characters in this recently described section was given by Zarre & Podlech (2002). The presence of long cylindrical hairs without papillae on the surface beside short flattened ones that are densely papillose on the surface is the most characteristic feature of this monotypic section. Astragalus semnanensis Sirj. & Rech.f. is exclusively white hairy and its calyx hairs are up to 3.5 mm long. The hairs on vegetative parts of the plant are up to 1.5 mm long and are so appressed to the bearing organs that they were considered to be medifixed (see Rechinger, Dulfer & Patzak, 1959; Maassoumi & Ranjbar, 1998). Similarly to A. sect. Microphysa, the hairs are exclusively white and short (up to 2 mm), even on the calyx. Some species, e.g. A. baba-alliar Parsa, are glabrous or sparsely hairy on the calyx and ovary, a character which relates this species to A. sect. Eriostoma. In this section the hairs are partly cylindrical-filiform and partly ribbon-like and flattened. However, in both cases they are densely papillose on the surface. Unlike in A. sect. Acanthophace, the flattened hairs in this section are not necessarily short. A detailed taxonomic description of the species in this section is presented by Tietz (1988). A detailed taxonomic description for the two species of this section was presented by Podlech (1975). The hairs in this section are white mixed with black in the region of the inflorescence. They are up to 1.5 mm on vegetative parts and up to 4 mm on the calyx. Astragalus stipitatus Bunge is covered by flattened ribbon-like hairs which are densely papillose on the surface. These hairs in contrast to A. sect. Acanthophace and similarly to A. sect. Poterion are not appressed to the surface of the bearing organs. A. SECT. PTEROPHORUS DISCUSSION The hairs in this section are similar to A. sect. Rhacophorus. The species of this section resemble the species of A. sect. Rhacophorus. The only difference between these two sections is the presence of two filiform bracteoles at the base of calyx in A. sect. Pterophorus (Zarre, 2000). In accordance with this similarity, the type of indumentum is the same in both sections. Today the phylogenetic systematics of Astragalus is more or less restricted to molecular approaches. The results of genome analysis, such as rpoC (Liston & Wheeler, 1994), ITS and chloroplast DNA trnL intron data (Wojciechowski, Sanderson & Hu, 1999) are not concerned in depth with subgeneric classification in Astragalus. Because of a high level of homoplasy with respect to macromorphological characters (Zarre, A. SECT. STIPITELLA (FIG. 26) © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 A. SECT. MICROPHYSA (FIG. 21) A. SECT. RHACOPHORUS (FIG. 24) With about 70 species worldwide, this section is the largest one among thorny Astragalus. The hairs are very variable in length in this section. In some species, e.g. A. zoharyi Eig, the longest hairs on the calyx do not exceed 1.5 mm, while in some species, e.g. A. stenolepis Fisch. the calyx hairs can reach 6 mm. However, in most species an intermediate size of about 4.5 mm on the calyx is more frequent. In several species, especially those with small flowers, the calyx is glabrous at its base, but very densely villous further up. This feature was used earlier for separation of the sections Platonychium and Stenonychium from this section. The hairs in this section are exclusively white and not papillose or very sparsely papillose on surface. They are cylindrical-filiform. HAIRS IN THORNY ASTRAGALUS SPECIES 24 25 26 Figures 23–26. Leaf hairs in Astragalus sect. Poterion (Fig. 23). A. sect. Rhacophorus (Fig. 24). A. sect. Semnanenses (Fig. 25) and A. sect. Stipitella (Fig. 26). Fig. 23. A. spinosus. Scale bar = 200 mm. Fig. 24. A. dissectus. Scale bar = 200 mm. Fig. 25. A. semnanensis. Scale bar = 100 mm. Fig. 26. A. stipitatus. Scale bar = 100 mm. 2000), it is necessary to take other characters such as micromorphological ones into consideration. Although many characters relating to hairs can be strongly influenced by ecological conditions, others provide constant features within certain species or sections. This study shows that several characters of hairs can be used for phylogeny reconstruction in Astragalus. The following sections of thorny Astragalus possess white hairs mixed with black ones, at least in the region of inflorescence: A. sect. Acanthophace, A. sect. Adiaspastus, A. sect. Aegacantha, A. sect. Anthylloidei and A. sect. Stipitella. In the first two sections the pods are bilocular and woody in texture. In A. sect. Adiaspastus and A. sect. Anthylloidei black hairs are present in a group of species which are known as most primitive in these sections (see Zarre, 2000, 2001a). Other symplesiomorphies known in combination with black hairs in these sections are: woody pods, a standard not differentiated into claw and limbs and nonrupturing fruiting calyx. The character ‘hair colour’ can be considered as a reliable one in assessing phylogenetic relationships between closely related species or the species within one section. Flattened ribbon-like hairs are characteristic for A. sect. Acanthophace (Zarre, 2000; Zarre & Podlech, 2001b). These hairs are also present in A. semnanensis, interestingly very densely on leaves and very sparsely on the calyx (Fig. 25). The replacement of flattened hairs by cylindrical-filiform ones at a late stage of plant development, is considered ontogenetic evidence against the primitiveness of this type of hair. Moreover, such hairs are also characteristic of several members of subtribe Coluteinae (sensu Polhill, 1981), which show close relationships to Astragalus (see Zarre, 2000). Another hair feature with phylogenetic importance is the presence or absence of papillae on the hair surface. The flattened hairs are always densely papillose on the surface, while cylindrical-filiform ones in some species can be papillose and in others not so. Hairs with a smooth surface are rare. Those with striate surfaces are frequent when papillae are absent or sparsely present on the hair surface. The sections with cylindrical-filiform hairs in combination with papillae are: A. sect. Aegacantha, A. sect. Anthylloidei (e.g. A. noziensis and A. lumsdenianus) and A. sect. Poterion. This type of hair can also be observed in some species of Oxytropis, the sister group of Astragalus. As the presence of papillae on the hair surface is also characteristic of almost all members of © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 23 329 330 S. ZARRE Coluteinae (Zarre, 2000), it also seems to be an ancestral character. ACKNOWLEDGEMENTS REFERENCES Bunge A. 1868–1869. Generis Astragali Species Gerontogeae. Mémoires L’Académie Impériale des Sciences de Saint Pétersbourg, Série 7, 11(16): 1–140 and 15(1): 1–245. Deml I. 1972. Revision der Sektionen Acanthophace Bunge und Aegacantha Bunge der Gattung Astragalus L. Boissiera 21: 1–235. Duman H, Vural M. 1990. New taxa from South Anatolia, I. Doga Turkish Journal of Botany 14: 39–48. Liston A, Wheeler JA. 1994. The phylogenetic position of the genus Astragalus (Fabaceae): Evidence from the chloroplast genes rpoC1 and rpoC2. Biochemical Systematics and Ecology 22: 377–388. Maassoumi AA, Ranjbar M. 1998. Revision of the genus Astragalus L: sect. Leucocercis Bunge (Leguminosae) from Iran. Iranian Journal of Botany 7(2): 239–248. Podlech D. 1975. Revision der Sektion Stipitella G. Grig. ex Podlech der Gattung Astragalus L. Mitteilungen der Botanischen Staatssammlungen München 12: 33–50. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 323–330 Downloaded from https://academic.oup.com/botlinnean/article/143/3/323/2433569 by guest on 11 March 2023 I am grateful to Mrs Eva Facher (Munich) for her assistance in providing the scanning electron micrographs. Prof. Dr D. Podlech (Munich) and Dr A. A. Maassoumi (Tehran) helped me by their useful comments and suggestions. I also thank the curators of the Institut für Systematische Botanik der Universität München for the loan of herbarium material and other help. This paper was supported by the project number 513/4/580 ‘Morphological and Systematic Studies on some Sections of the Genus Astragalus (Fabaceae)’ of the Research Council of Tehran University. Podlech D. 1982. Neue Aspekte zur Evolution und Gliederung der Gattung Astragalus L. (Leguminosae). Mitteilungen der Botanischen Staatssammlungen München 29: 461–469. Polhill RM. 1981. Tribe 16. Galegeae. In: Polhill RM, Raven PH, eds. Advances in legume systematics. 1. Kew: Royal Botanic Garden, 357–363. Rechinger KH, Dulfer H, Patzak K. 1959. S irjaevii fragmenta astralogica XI. Sect. Leucocercis. Österreichische Akademie der Wissenschaften, Sitzung der Mathematisch-Naturwissenschaftlichen Klasse, Sitzungsbericht 1, Biologie 168/8–9: 714–718. Tietz S. 1988. Revision von Astragalus L. sect. Campylanthus Bunge, sect. Microphysa Bunge und sect. Poterion Bunge. Mitteilungen der Botanischen Staatssammlungen München 27: 135–380. Tietz S, Zarre SH. 1994. Revision von Astragalus L. sect. Megalocystis Bunge (Fabaceae). Sendtnera 2: 287–363. Wojciechowski MF, Sanderson MJ, Hu J-M. 1999. Evidence on monophyly of Astragalus (Fabaceae) and its major subgroups based on nuclear ribosomal DNA ITS and chloroplast DNA trnL intron data. Systematic Botany 24 (3): 409–437. Zarre SH. 2000. Systematic revision of Astragalus sect. Adiaspastus, sect. Macrophyllium and sect. Pterophorus. Englera 18: 1–219. Zarre SH, Duman H. 1998. Notes on Astracantha marashica (Fabaceae). Sendtnera 5: 255–312. Zarre SH, Podlech D. 1996. Taxonomic Revision of Astragalus L. sect. Hymenostegis Bunge (Leguminosae). Sendtnera 3: 255–312. Zarre SH, Podlech D. 2001a. A short contribution to genus Astragalus L. (Fabaceae) in Turkey. Pakistan Journal of Botany 33 (2): 153–155. Zarre SH, Podlech D. 2001b. Taxonomic Revision of Astragalus sect. Acanthophace (Fabaceae). Sendtnera 7: 233–255. Zarre SH, Podlech D. 2002. Astragalus sect. Semnanenses (Fabaceae): a new monotypic section from Iran. Nordic Journal of Botany 21 (5): 485–491.