Aster Amellus L. (Asteraceae)

G Model PPEES-25121; No. of Pages 12 ARTICLE IN PRESS

Perspectives in Plant Ecology, Evolution and Systematics xxx (2011) xxx–xxx

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Perspectives in Plant Ecology, Evolution and Systematics

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Biological Flora of Central Europe Biological ﬂora of Central Europe: Aster amellus L. (Asteraceae)

Zuzana Münzbergová a,b,∗, Jana Raabová c, Sílvia Castro a,d, Hana Pánková a a Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, 128 01 Prague, Czech Republic b Institute of Botany, Academy of Sciences, Zámek 1, 252 43 Pruhonice,˚ Czech Republic c Department of Botany, National Museum, Cirkusová 1740, 193 00 Praha 9, Czech Republic d CFE, Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal article info abstract

Article history: Aster amellus L. (Asteraceae) is a polymorphic aggregate of taxa. The species aggregate is distributed Received 18 May 2010 through Central and Eastern Europe and Western Asia. The habitats of the species include grasslands, Received in revised form 1 February 2011 clearings, edges, slopes, waysides and open forests. Typical habitats of this species have declined over the Accepted 14 March 2011 last decades, and A. amellus became endangered in many parts of Central Europe. This paper deals with taxonomy, morphology, distribution, habitat requirements, life cycle and biology of this species. Special Keywords: emphasis is given to the differences between diploid and hexaploid plants, which co-occur in Central Central Europe Europe. Ecology Flow cytometry © 2011 Elsevier GmbH. All rights reserved. Genetics Polyploidy Species biology

Taxonomy and morphology A. amellus is the type species for the genus Aster, family Aster- aceae and order Asterales (Jones, 1980; Pennisi, 2001). The name Taxonomy Aster comes from the Ancient Greek word astér, which means “star” and refers to the shape of the flower head. Aster s.l. is a mor- Aster amellus L. Sp. Pl. 873, 1753 (Asteraceae) – Italian aster phologically heterogeneous and geographically widespread genus, Heterotypic synonyms: comprising over 400 species, with centres of diversity in North Aster amelloides Hoffm. Gött. Anz. Gel. Sachen 20: 1325, 1800. America and Eurasia. The genus has a complex taxonomic history, – Aster ottomanus Velen. Sitzungsber. Königl. Böhm. Ges. Wiss., with several partial taxonomic treatments attempting to iden- Math.-Naturwiss. Cl., 1890: 48, 1890. tify natural groups (reviewed in Jones, 1980; Jones and Hiepko, Aster bessarabicus Rchb. Fl. Germ. Excurs. 246, 1831–1832. – 1981; Nesom, 1994a; Xiang and Semple, 1996). Recent morpho- Aster amellus subsp. bessarabicus (Rchb.) Soó Acta Bot. Acad. Sci. logic and molecular studies revealed that the genus is generally Hung. 12: 366, 1966. – Aster scepusiensis Kitaibel ex Kanitz Linnaea restricted to the Old World species (Aster s.s. with about 180 32: 373, 1863. – Aster amellus subsp. scepusiensis (Kanitz) Dostál species; Nesom, 1994a,b; Noyes and Rieseberg, 1999), and most of Folia Mus. Rerum Natur. Bohem. Occid., Bot., 21: 12, 1984. – Aster the North American asters belong to other related genera (Nesom, amelloides Besser Enum. Pl. 33, 1821 [non Hoffm. 1800], homonym. 1994b; Xiang and Semple, 1996; Noyes and Rieseberg, 1999). Phy- Aster ibericus M. Bieb. Fl. Taur.-Caucas. 2: 311, 1808. – Aster amel- logenetic studies based on nucleotide sequence data from the lus subsp. ibericus (M. Bieb.) V.E. Avet. Biol. Zurn.ˇ Armenii 25(10): internal transcribed spacers (ITS) of nuclear ribosomal DNA and 63, 1972. amplified fragment length polymorphism (AFLP) markers suggest Aster hirtus K. Koch Linnaea 23: 701, 1851 [non Scop. 1772]. – that Old World Aster is a polyphyletic group, with independent lin- Aster elegans Willd. Sp. Pl., ed. 4 [Willd.] 3(3): 2042, 1803. – Amellus eages derived from possibly distant southern hemisphere ancestors officinalis Gaterau Fl. Montauban 147, 1789, nom. illeg. – Amellus (Noyes and Rieseberg, 1999; Cammareri et al., 2004). vulgaris Opiz Sezn. Rostl. Kvet.ˇ Ces.ˇ 14, 1852, nom. illeg. Phylogenetic and cladistic studies performed so far within the genus Aster reveal a close relationship between A. amellus and A. alpinus (AFLP analysis, Cammareri et al., 2004; cladistic analysis, Jones and Young, 1983; Nesom, 1994a). Xiang and Semple (1996) ∗ Corresponding author at: Department of Botany, Faculty of Science, Charles Uni- found different phylogenetic relationships within Aster based on versity in Prague, Benátská 2, 128 01 Prague, Czech Republic. Tel.: +420 221 951 636; divergence of cpDNA. This classification is, however, suspicious as fax: +420 221 951 645. E-mail address: [email protected] (Z. Münzbergová). the sample of A. amellus used in the study of Xiang and Semple

Please cite this article in press as: Münzbergová, Z., et al., Biological ﬂora of Central Europe: Aster amellus L. (Asteraceae). Perspect. Plant Ecol. Evol. Syst. (2011), doi:10.1016/j.ppees.2011.03.002 G Model PPEES-25121; No. of Pages 12 ARTICLE IN PRESS

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(1996) was an octoploid plant from a garden in Quebec, Canada and els cannot be morphologically distinguished. A molecular approach it may in fact be a hybrid of A. amellus with some Eurybia species. also revealed that the two cytotypes cannot be distinguished based A. amellus (Fig. 1) is a polymorphic aggregate of taxa, includ- on isozyme profiles, thus sharing a common gene pool (Mandáková ing three cytotypes: diploids (2n =2x = 18), tetraploids (2n =4x = 36) and Münzbergová, 2008). The two cytotypes are also not separated and hexaploids (2n =6x = 54) (Merxmüller et al., 1976; Májovsky,´ based on cpDNA (Castro et al., unpubl.). Castro et al. (unpubl.) dis- 1978). The aggregate of the species has received several taxonomic tinguished until now four major clades in Central Europe, where treatments based on both morphological and caryological charac- two clades contained both diploid and hexaploid individuals, sug- ters. Tamamshyan (1990) and Májovsky´ (1978) distinguished three gesting multiple independent origin of hexaploids. These results independent taxa within the aggregate: A. amellus L., A. ibericus support the treatment of Aster amellus as one polymorphic species Stev. and A. amelloides Bess. non Hoffm. instead of multiple independent taxa. According to Májovsky´ (1978) the classification of the species Hegi (1979) indicates that the species is very variable in its leaf as three independent taxa is justified by their morphological dif- shape and hairs without any needs to distinguish new taxa. Some ferences, different chromosome numbers, distinct expected areas plants with reddish edge of involucral bracts were described as f. of origin and different evolutionary histories. Following Májovsky´ lauticeps Beck and similarly plants with strongly pubescent leaves (1978), A. amellus L. includes diploid plants with small heads and were described as var. hispidus DC. However, the taxonomic value oval obtuse involucral bracts, distributed from sub-Mediterranean of these forms is doubtful (Hegi, 1979). to temperate sub-continental Europe and to western Siberia. A. Due to the unclear taxonomical treatment of this group and ibericus Stev. includes tetraploid plants with big heads, long disk- to the recent morphological and molecular studies (Mandáková florets and lanceolate acute hairy involucral bracts, distributed and Münzbergová, 2008), we use a conservative approach, fol- from sub-Mediterranean mountains to sub-temperate western lowed also in Flora Europaea (Merxmüller et al., 1976), and consider Asia. A. amelloides Bess. non Hoffm. includes hexaploid plants with A. amellus as a polymorphic species, including all the cytotypes, big heads and lanceolate acute glabrous involucral bracts, dis- through the paper. Lot of biological data on A. amellus is available tributed from sub-Mediterranean via sub-temperate to eastern only from limited geographic area of this species, not including sub-continental Europe and to western Asia. all ploidy levels and subspecies. Because we are aware of the lim- Contrary to Májovsky´ (1978), studies on chromosome counts itations of these findings for the whole aggregate of the taxa, we of these species (Huziwara, 1962; Magulaev, 1986) report that A. always report the geographic area of the specific studies. For exam- amellus L. are diploid plants, and A. ibericus Stev. and A. amelloides ple, comparisons of habitats, life cycle, phenology and reproduction Bess. non Hoffm. are both hexaploid plants. between diploid and hexaploid plants come mainly from our own Tamamshyan (1990) does not report the ploidy level of the research on A. amellus in the Czech Republic. three taxa, but distinguishes the same three taxa as Májovsky´ (1978) based on plant morphology. According to Tamamshyan Morphology (1990), A. amellus plants are glabrous or subglabrous. The outer bracts of involucre are subglabrous. Inner bracts are lanceolate Description of plant morphology is given for the whole polymor- and both types of bracts are coloured. Lower leaves are elliptic- phic A. amellus species. Where the information is available, we also spathulate and the stem is often reddish. In contrast, A. amelloides provide separate information for diploid and hexaploid cytotypes and A. ibericus are strongly pubescent and scabrous. Outer bracts based on our own data (no information on tetraploid cytotype is of involucre are acute and more or less pubescent. A. amelloides are available, see Section ‘Chromosome numbers’). green subglabrous plants with numerous flower heads, 16–20 mm in diameter. Bracts of involucres are rigidate, dorsally rough-haired. Plant description A. ibericus plants are greyish green with dense pubescence. The Aster amellus is a hemicryptophyte perennial herb (Fig. 1a) with heads are less numerous than at A. amelloides and larger (30–50 mm an oblique to horizontal rhizome. In the vegetative stage, the plant in diameter). Bracts of involucres are dorsally more densely bristly produces semi-rosettes with several long leaves attenuated in a pubescent, usually not coloured and acute. petiole (Fig. 1e). In sexual stage, one genet produces one to several According to Flora of Russia (Tzvelev, 2002), A. amellus includes pubescent sympodial stems (ramets) (means ± SD: 1.75 ± 2.4 for three subspecies, which correspond to the three species distin- diploids, 2.24 ± 3.45 for hexaploids), 10–80 cm high (means ± SD: guished above (see Synonyms): A. amellus subsp. amellus, A. amellus 35.5 ± 13.56 for diploids, 42.24 ± 16.63 for hexaploids); stems are subsp. ibericus (Stev.) Avetisjan, and A. amellus subsp. bessarabicus straight and often decumbent at the base, simple or branched (Rchb.) Soó. This classification at the level of subspecies was used above, leafy along all the length, sometimes reddish. Basal and also by Meusel and Jäger (1992), who provided the distribution map lower cauline leaves are rough, up to 12 cm long (means ± SD: of the three subspecies of A. amellus. 3.45 ± 1.58 for diploids, 4.24 ± 1.46 for hexaploids) and up to Kovanda (2002) performed cytological and morphological 4 cm wide (means ± SD: 0.79 ± 0.35 for diploids, 0.93 ± 0.43 for studies on A. amellus in Central Europe and reported two morpho- hexaploids), broadly lanceolate, obovate or spathulate and elon- logically, cytologically and distributionally distinct taxa from the gated into very short petiole, 3-nerved and with margin entire. Czech Republic: diploid A. amellus L. and hexaploid A. scepusiensis Middle and upper cauline leaves are oblong to lanceolate, sessile, Kitaibel ex Kanitz (correct name A. amellus L. subsp. bessarabi- 3-nerved and become smaller towards the top. The leaves on the cus (Rchb.) Soó). This taxonomical treatment was also adopted young rosettes are distichous. In contrast, the leaves at the flow- in the Flora of the Czech Republic (Kovanda, 2005). However, ering stalks are scattered (Troll, 1937–1941). The leaves are rough recent studies performed by Mandáková and Münzbergová (2006) hairy on both sides, with archly bent, more or less pressed hairs, demonstrated that diploid and hexaploid populations are largely rarely (particularly on the top) glabrous (Hegi, 1979). intermixed within the Czech Republic, contrarily to the clear dis- Capitula are between 3 and 5 cm in diameter and arranged in tributional patterns described by Kovanda (2002). In a subsequent simple corymbs or umbel-like panicles (Fig. 1b) (number of flow- study, Mandáková and Münzbergová (2008) compared morpho- erheads per ramet, means ± SD: 4.62 ± 3.91 for diploids, 5.19 ± 4.3 logical characters of diploid and hexaploid plants collected in the for hexaploids). Involucral bracts are rough, displayed in 2–4 rows, field as well as diploid and hexaploid plants cultivated from seeds in the outer bracts shorter than the inner ones, spathulate to obtuse. an experimental garden and demonstrated that the two ploidy lev- Each flower head is composed by an external row of female ligulate

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Fig. 1. Aster amellus L. (Asteraceae): (a) plant habit (A. amellus,2×); (b) detail of the inﬂorescences (A. amellus,2×); (c) pollinator Eristalis sp. (Diptera) visiting the ﬂower head of A. amellus (6×); (d) detail of the infrutescence (A. amellus,2×); (e) whole plant showing the root system (A. amellus,2×).

flowers and central yellow tubular and hermaphroditic flowers. and Landolt et al. (2010) reports from Switzerland that roots of A. Ligulate flowers have ligula between 5 and 15 mm long and a short amellus can reach up to 50–100 cm deep. Clearly, the rooting depth tube. The whole ligulate flowers are 10.56 ± 7.71 mm for diploids, strongly depends on soil conditions at each particular locality and 15.01 ± 11.41 mm for hexaploids, long. The ligulate flowers are can range from a few centimetres at extreme rocky localities up to linear-lanceolate and blue to violet, rarely white or red coloured. over a meter at very deep soils. The ligular flowers are 3-lobed representing true rays (Bremer, Ratio of aboveground to belowground fresh mass is 1.4 (range 1996). Tubular flowers are hermaphrodite, yellow, 5–6 mm long. 1.0–1.9) in dry grasslands in Germany, which corresponds to the Total number of florets within a single flower head is 69 ± 14 average values for plants from the same habitat (Müller-Stoll, (mean ± SD) for diploid plants and 79 ± 20 for hexaploids. 1935). The diaspores are achenes (Fig. 1d), which are 2–4 mm ± ± long (2.76 2.11 for diploids, 2.80 0.33 for hexaploids) and Pollen morphology ± ± about 1–1.5 mm wide (1.38 0.20 mm and 1.31 0.16 mm for Morphology of pollen of Asteraceae from Europe has been diploids and hexaploids, respectively). The achenes are covered recently reviewed by Punt and Hoen (2009). The pollen of A. amel- with compressed dense yellowish to reddish or brown hairs. lus is included within the A. tripolium type and is a combination ± Pappus-hairs are longer than achene (3.84 0.48 mm for diploids, of Aster type of Erdtman et al. (1961) and van den Assem (1968) ± 4.99 0.77 mm for hexaploids) whitish to reddish. Fully developed and the Eupatorium type of Stix (1960). The pollen grains are 3- ± seeds of diploid plants are lighter (1.01 0.28 mg) than seeds of zonocolporate, oblate spheroidal to prolate spheroidal. A. amellus ± hexaploid plants (1.19 0.25 mg). pollen have mean polar axis (P) of 23.5 ␮m (ranging from 23.0 to In spite of the difference in number of florets between diploid 25.0 ␮m), mean equatorial axis (E) of 24.5 ␮m (ranging from 23.0 to and hexaploid cytotype, there is no significant difference in num- 26.0 ␮m) and mean P/E ratio of 0.97 (ranging from 0.96 to 0.99; all ± ber of developed seeds between the two ploidy levels (mean SD: measurements in silicone oil preparations) (Punt and Hoen, 2009). 55 ± 18.6 and 56 ± 23.5 for diploids and hexaploids, respectively). This is due to higher seed predation rate as well as higher seed Distribution and habitat requirements abortion rate in the hexaploid plants (Münzbergová, 2007a; Castro et al., 2011). Geographical distribution Unless specified otherwise above, the plant description is based on Merxmüller et al. (1976), Hegi (1979), Tamamshyan (1990) and Distribution in the native range Klimesováˇ and de Bello (2009), the differences between diploids Aster amellus L. is mainly a European species. The general and hexaploids are based on Mandáková and Münzbergová (2008) native distribution extends from the northern French depart- and our unpublished data. ments Champagne-Ardenne and Lorraine, over Rhineland-Palatine to Thuringia in Central Germany. Over the relatively dry warm Root system Bohemian and Moravian basins the Northern range border Aster amellus creates high amount of roots at the bases of each stretches to S-Poland, N-Ukrainia, and adjacent Russia to Tatarstan new vegetative shoot resulting in very dense root system (Troll, and the Permsk Oblast in the Northeast. From there it reaches 1964)(Fig. 1e). The majority of the roots can be found in the upper southwards along the Ural mountains over S-Bashkortostan and 30 cm of the soil (pers. obs.). At rocky localities, most of the roots the Volgograd Oblast to the Caucasus Mountains in the Southeast. are in the upper 10 cm (pers. obs.). Similarly, Müller-Stoll (1935) The southern distribution limit stretches over Central Ukrainia and reports the mean depth of A. amellus roots of 25 cm (range 18–30 cm S-Bulgaria along the Adriatic coast to N-Italy, and South-Central and 15–25 cm for the main and lateral branches respectively in France, where the species supposedly has its south-westernmost the hills of south-west Germany, Kreichgauer Hügelland). Golubev occurrences in the department Languedoc (Fig. 2, Welk unpubl.). (1962), however, reported from forested steppes in Russia that Within the continuous continental European distribution range, roots of A. amellus can reach up to 2.21 m deep and laterally extend A. amellus is largely missing in a large gap in the Great Hungarian up over 1 m. Similarly, Lichtenegger (1976) reported that roots of Plain, where the predominating sandy soils are partly salinized. A. amellus can reach the depth of 87 cm on deep Pararendzina soil Further distribution gaps are located in several montane regions

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Fig. 2. Complete distribution of A. amellus. Black dots represent native occurrences; open circles represent synanthropic occurrences; hatched areas represent the more or less continuously populated distribution range. probably because parent material consists largely of acidic granite which deserves more detailed research in the future (Castro et al., and gneissose rocks. Since A. amellus prefers base rich, calcareous unpubl.). soils, the species is limited towards the North rather by edaphi- Szafer (1959) considers A. amellus in Poland to be an early cally unsuitable pleistocene soils, than by clear climatic limitations. Holocene relict species similarly to Inula hirta, Adenophora liliifolia Especially the northern distribution limit in S-Netherlands, Central and Trifolium lupinaster. Germany, and S-Poland seems not correlated with climatic factors. Here, the native distribution might be limited mainly edaphically Distribution in the secondary range and cultivation due to acidic infertile soils of pleistocene origin (Welk unpubl.). A. amellus is a commonly cultivated and commercialized species. The northernmost outposts at this distribution limit are located The first record of cultivation of A. amellus comes from England in hilly landscapes or at the margin of river valleys on base rich from 1596 (Parkinson, 1976). Since then the species is widely parent material like calcareous rocks or loess. At the southern cultivated in many areas of the world and there are many gar- distribution limit, A. amellus is increasingly confined to montane den cultivars and hybrids available on the market (e.g., Picton, habitats where mean summer precipitation is above 120 mm. The 2005; web 1 http://members.tripod.com/∼hatch l/aste3040.html southern distribution limit in Eastern Europe is caused primarily (accessed 04.12.09)). by climate (water balance, precipitation of wettest month <60 mm, Outside the native area, A. amellus was recorded as naturalized Welk unpubl.). in 1944 at a single location in New Zealand (Webb, 1987). No further Concerning ploidy distribution patterns, the three cytotypes information on naturalization of A. amellus from cultivation was have been described to be geographically separated. The available described up to now. It thus seems that the cultivated A. amellus references report the occurrence of diploids in the central- generally does not escape to wild and does not interact with natural , west- and south-European populations (Holub et al., 1970; populations. Pogan and Rychlewski, 1980; Rostovtseva, 1983; Kovanda, 1984, Cammareri et al. (2001) demonstrated that A. amellus can be 2002; Krahulcová, 1990; Tamamshyan, 1990; Wisskirchen and relatively easily propagated by in vitro cultures. In fact, A. amellus Haeupler, 1998; Mandáková and Münzbergová, 2006). In con- was one of the best in growth in vitro culture when compared to trast, hexaploids are reported mainly in continental part of Eurasia 15 other species of Aster. and but also in central- and east-European populations (Löve, 1974; Májovsky,´ 1978; Dvorak and Dadáková, 1974; Micieta,ˇ 1981; Habitat Tamamshyan, 1990; Meusel and Jäger, 1992; Kovanda, 2002; Mandáková and Münzbergová, 2006). Tetraploids should occur Aster amellus is a heliophilous to semi-heliophilous species with from sub-Mediterranean mountains to sub-temperate western CS strategy according to publication of Frank and Klotz (1990) Asia (Májovsky,´ 1978). for Germany or CSR strategy according to publication of Landolt Recent large scale cytotype screenings in Central Europe using et al. (2010) for Switzerland, occurring in montane mesophilous flow cytometry revealed that diploid and hexaploid populations broad-leaved forest belt (Borhidi, 1995). It is strongly urbanopho- have a complex and diffuse contact zone through the Czech Repub- bic species (Landolt et al., 2010). It grows in warm hilly to montane lic, Slovakia, Poland and Austria (Mandáková and Münzbergová, areas on limestone substrates with carbonated to eutrophic humus 2006; Castro el al. unpubl.). There, diploid and hexaploid plants and basic to neutral pH (Table 1). It occurs predominantly in colline occur in close proximity, but never form mixed populations and only sporadically in montance belt (e.g., up to 1630 m a.s.l (Mandáková and Münzbergová, 2006). Recently, one mixed popu- in Graubünden in Swiss Alps, up to 1420 m a.s.l in Tirol, Austria lation has been found in Austria close to the border with Hungary, and up to 1200 m a.s.l. in Kärnten, Austria; Hegi, 1979). It is a

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mesophilic to xerophilic species. The habitats of the species in France and Switzerland include grasslands, clearings, forest edges, slopes, waysides and open pine and oak forests (Rameau et al., . 1989; Landolt et al., 2010). In central Europe, it mainly occurs at forest edges (at the border of dry grasslands and sunny forests; capacity (%) Hegi, 1979; Chytry´ et al., 2001). The substrate materials are gravel, calcareous sand, clay, loess and silts (Hegi, 1979). According to indicator values developed for the ﬂora of Germany (Ellenberg et al., 1992), Hungary (Borhidi, 1995), Switzerland Raabová et al. (2008) (Landolt et al., 2010) and Poland (Zarzycki et al., 2002) A. amellus is light demanding species (classiﬁed as half-light plant, i.e. mostly growing in full light but being shadow tolerant, by Borhidi, 1995

and Fig. 1 in and Landolt et al., 2010), occurring on relatively warm basiphilous continental (subcontinental) habitats. It requires semi dry habitats (with very fluctuating moisture content) with low soil fertility and medium humus content. It is able to grow in badly aerated soils. It does not tolerate saline soils. In the Czech Republic, habitats of diploid and hexaploid populations do not significantly differ in mean Ellenberg indi- Raabová et al. (2007) cator values and potential direct solar irradiation (Mandáková and Münzbergová, 2006). However, they differ in habitat productivity. Hexaploid populations occur in both low- and high- productive habitats, whereas diploid populations are confined to low-productive habitats (Mandáková and Münzbergová, 2006; Münzbergová, 2007b). Multivariate analyses including nine neigh- bouring populations of A. amellus in the Czech Republic showed that the sites of diploid and hexaploid populations differ significantly in soil properties and vegetation composition (Raabová et al., 2008). And a series of reciprocal transplant experiments among the

g/g) Total N (%) Total C (%) Carbonates (%) Organic C (%) C/N ratio Water holding Czech populations indicates niche differentiation between the two ␮ ploidy levels (Raabová et al., 2008) and local adaptation both in diploids and hexaploids (Raabová et al., 2007, 2008). Nevertheless, diploid plants were able to grow in the hexaploid localities and vice g/g) K (

␮ versa, indicating overlap in habitat requirements between diploid and hexaploid plants (Raabová et al., 2008).

Communities

The species occurs in several major vegetation types including

in the Czech Republic. For methods and population codes see Table 1 in meso-xerophilous grasslands on deep calcareous soils (Bromet-

O) Ca (mg/g) Mg ( alia erecti), sub-continental to continental closed fescue pastures 2 and swards (Festucetalia valesiacae), open xerophilous rocky grasslands of sunny aspects of central and south-eastern Europe (Stipo

Aster amellus pulcherrimae-Festucetalia pallentis), dealpine, closed, blue-grass dominated grasslands of the Alps, Hercynicum and Carpathi- ans (Seslerietalia rigidae), herbaceous vegetation on woodland margins and ridges on calcareous soils (Origanetalia vulgaris), 222 5.442 6.20 4.68 7.74 4.98 7.86 191.04 10.84 737.73 271.46 8.25 299.38 0.44 217.49 282.86 0.46 74.74 0.53 6.55 167.70 6.516 0.20 0.02 10.22 0.03 2.96 8.20 7.58 6.53 6.20 6.48 5.27 7.26 15.00 93.39 2.00 14.23 38.11 13.61 266.20 31.28 42.10 0.30 9.87 44.33 4.10 0.40 3.70 11.30 39.73 226 7.846 8.056 9.71 7.656 9.36 7.59 80.076 9.11 7.87 37.32 10.19 180.40 7.65 61.03 0.30 6.05 82.89 7.71 68.97 124.50 6.97 0.10 76.03 217.30 0.20 8.90 7.35 106.93 0.20 118.00 8.30 5.20 88.47 218.50 0.10 4.50 6.40 0.30 5.20 219.90 1.20 0.20 4.10 3.70 2.80 5.90 1.90 2.60 4.90 3.30 14.10 1.90 2.40 15.70 42.04 2.20 1.40 14.00 52.40 4.00 10.60 40.50 2.70 10.20 35.89 12.60 40.85 11.40 43.64 39.81 sub-scrub and scrub vegetation seral or marginal to broad- leaved woodland (Prunetalia spinosae), xerothermophilous forests (Quercetalia pubescenti-petraeae), calcareous relict montane pine N N E E E E E E E N E E E E E N N N N N N N N N woods (Erico-Pinetalia) and thermophilous inner alpine woods 01 52 02 56 49 33 58 41 23 51 57 10 29 16 24 16 41 46 36 56 46 03 15 15 with undergrowth of steppic character (Astragalo monspessulani- 56 07 56 15 59 20 05 13 15 18 18 18 17 17 18 32 31 31 30 29 27 30 30 29 Pinetalia sylvestris)(Table 2, description of the communities ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ according to Rodwell et al., 2002). A. amellus is diagnostic species for 14 14 14 14 14 14 14 14 14 14 14 14 associations of Cirsio-Brachypodion pinnati (Moravec et al., 1995) and Astero amelli-Rosenion pimpinellifoliae (Julve, 2006).

Response to abiotic factors

Response to abiotic factors of A. amellus was studied with transplant experiments in the ﬁeld and common garden in the Czech Republic and Germany. In the ﬁeld experiments in the Czech Republic, germination percentage, survival probability and plant size varied among six studied sites, which differed in potential Population RegionK1 Coordinates Czech Karst 49 Ploidy level pH (H K2K3S1 Czech KarstS2 Czech Karst 49 Ceske Stredohori 49 50 Ceske Stredohori 50 S3S4S5 Ceske Stredohori 50 S6 Ceske Stredohori 50 S7 Ceske Stredohori 50 S8 Ceske Stredohori 50 S9 Ceske Stredohori 50 Ceske Stredohori 50 Ceske Stredohori 50

Table 1 Mean soil properties of soil taken from the upper 20 cm from 12 sites of direct solar irradiation and soil properties (Raabová et al., 2007).

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Table 2 lus depend on environmental conditions. The species builds rather Syntaxonomical units with occurrences of Aster amellus, based on Szafer (1959), sparse stands when growing in open forest, but the density might van Gils et al. (1975), Soó (1970), Oberdorfer (1978, 1994), Guinochet and Vilmorin (1982), Mayer (1982), Rameau et al. (1989), Donita˘ et al. (1992), Mucina et al. (1993), be higher when the conditions are suitable, for example in open 2 Moravec et al. (1995), Ellenberg (1996), Delarze et al. (1998), CBNBP-Délégation grasslands, with up to 7.5 flowering individuals per 1 m (Mayor, Centre (2000), Schubert et al. (1995, 2001), Stanová and Valachovicˇ (2002), Chytry´ 2008). (1997, 2007), Czarnecka (2004), Julve (2006), Galasso and Selvi (2007), Fischer et al. (2008), Mayor (2008) and Landolt et al. (2010). The names of the syntaxons do not match the original publications as they were all unified according to Rodwell et al. Life cycle and biology (2002) to fit into a common system. Entries in [ ] denote geographic origin of the information (AU – Austria, CH – Switzerland, Cr – Crimea, Part of Ukraine, CZ – Czech Republic, FR – France, GE – Germany, HU – Hungary, IT – Italy, PO – Poland, RO – Life cycle Romania, SK – Slovakia, SLO – Slovenia, and UKR – Ukraine). Three basic stages can be distinguished in the life cycle of Festuco-Brometea [AU, Cr, CH, CZ, FR, GE, HU, PO, RO, SLO] Brometalia erecti [AU, CH, CZ, FR, GE, PO, RO, SLO] the species: seedlings, vegetative plants, and reproductive plants. Cirsio-Brachypodion pinnati [AU, CZ, GE, PO, RO] Seedlings of A. amellus lose the cotyledons in very early stages of Bromion erecti [CH, CZ, GE, SLO] development, and cotyledons cannot be used to identify seedlings Festucetalia valesiacae [AU, CZ, HU, RO] in the field. The maximum leaf length that one individual can grow Festucion valesiacae [AU, CZ, HU, RO] within one year in the field in northern Bohemia, Czech Repub- Stipo pulcherrimae-Festucetalia pallentis [CZ, GE] Alysso saxatilis-Festucion pallentis [CZ] lic, is 3 cm. However, the plants can be smaller than 3 cm for up Xerobromion [GE] to several years in the field, depending on the climatic and habi- Seslerietalia rigidae [CZ] tat conditions. From the seedling stage, they can move either to Diantho lumnitzeri-Seslerion albicantis [CZ] a vegetative stage or directly to a flowering stage. A. amellus usu- Bromopsietalia cappadocicae [Cr] ally flowers in the second year after sowing in the common garden Adonido vernalis-Stipion tirsae [Cr] Trifolio-Geranietea sanguinei [CH, CZ, FR, GE, HU, SLO] when watered regularly, but some individuals may already flower Origanetalia vulgaris [CH, CZ, FR, GE, HU, SLO] in the first year when kept in the greenhouse over the vegetation Geranion sanguinei [CH, CZ, FR, GE, HU, SLO] season. In the field it takes at least 3, but usually about 5–7 or even Trifolion medii [CZ] more years to flower. From flowering stage, plants can get back to Quercetea pubescentis [CH, CZ, FR, IT, UKR] Quercetalia pubescenti-petraeae [CH, CZ, FR, IT, UKR] vegetative. Both vegetative and reproductive plants can reproduce Quercion petraeae [CZ] also clonally (Münzbergová, 2007a, see section on ‘Clonal growth’ Quercion pubescenti-sessiliflorae [CH, FR] for details). Carpinion orientalis [IT] The mean performance of different ploidy levels in the Czech Rhamno-Prunetea [FR] Republic does not significantly differ in the field (Münzbergová, Prunetalia spinosae [FR] Berberidion vulgaris [FR] 2007a; Raabová et al., 2008). However, a simulated population Erico-Pinetea [FR, GE, CH] of 100 flowering individuals of diploids had 0.4% probability to Erico-Pinetalia [FR, GE, CH] become extinct in 20 years and 27% probability to become extinct Erico-Pinion sylvestris [FR, GE, CH] in 50 years, while for hexaploid populations the probabilities were Pyrolo-Pinetea [CZ, SK] Astragalo monspessulani-Pinetalia sylvestris [CZ, SK] 4.5 and 70% (Münzbergová, 2007a). This is caused by higher effects Cytiso ruthenici- Pinion [CZ, SK] of demographic and environmental stochasticity on performance Querco-Fagetea [FR] of hexaploid populations and suggests that hexaploid populations Fagetalia sylvaticeae [FR] are more sensitive to extinction. Cephalanthero-Fagion [FR] Structure of population transition matrices describing whole life cycle of the species is different between diploids and hexaploids. There was a tendency for higher survival rates at sites with higher Namely, population growth rate of diploids is significantly driven potential direct solar irradiation (r = 0.78) and longer leaves at by generative reproduction, survival of vegetative individuals and sites with higher concentration of Ca2+ ions (r = 0.71). In a two- clonal growth, while population growth rate of the hexaploid pop- year garden experiment in the Czech Republic, plant performance ulations is driven mainly by the growth of vegetative plants to the differed between substrates from two different regions (Raabová flowering stage (Münzbergová, 2007a). et al., 2009). The response of A. amellus to these two substrates var- When comparing elasticity of different life cycle transition of ied among individual traits; while survival percentage was higher A. amellus with other species according to Silvertown et al. (1993), in the nutrient poorer but more basic substrate, the other traits A. amellus represents an extreme point among other iteroparous (number of stems, plant height, number of leaves, flowering per- herbs of open habitats, with very high elasticity of survival (0.85), centage, and number of flower heads) were higher in the nutrient medium elasticity for growth (0.13) and very low elasticity of richer but less basic substrate. In a three-year field experiment in reproduction (0.02, Münzbergová, 2007a). Germany, Kühn (2006) showed that number of flowering shoots Thanks to their clonal growth, the plants can be theoretically and survival percentage of A. amellus were higher when grown immortal. In the field conditions, the growth of the plants is very under rich soil conditions (pH, 6.3; N, 8.6 kg/ha; P, 37.3 mg/100 g; slow and their survival for many decades thus seems likely. In the and K, 18.1 mg/100 g) than under poor soil conditions (pH, 6.5; N, garden conditions, where the growth is much faster, the plants, 2.25 kg/ha; P, 27.1 mg/100 g; and K, 6.0 mg/100 g). however, tend to die within about 10 years (pers. obs.).

Abundance Spatial distribution of plants within populations

A. amellus occurs in populations of different sizes ranging from In a sowing experiment in both occupied and unoccupied local- few to tens of thousands of individuals (Münzbergová, 2006; ities of the species, Münzbergová (2004) showed that distribution Raabová et al., 2007; Mayor, 2008). The number of ﬂowering of the species is dispersal limited not only at the level of localities individuals in a population can vary among years depending on which are 1–20 km apart, but also at the level within localities at the weather conditions. Similarly, the densities of the stands of A. amel- scale of around 200 m. Within localities, the plants grow alone or

Z. Münzbergová et al. / Perspectives in Plant Ecology, Evolution and Systematics xxx (2011) xxx–xxx 7 in small groups (Landolt et al., 2010). For other information on spa- essentially an outcrosser. The success of self-pollinations is higher tial distribution see section ‘Abundance’ and section ‘Distribution in the hexaploids than in the diploids (Castro et al., 2011). of genetic variation within and between populations’. Pollinator assemblage and behaviour Phenology A. amellus is an enthomophilous species pollinated by a wide and diverse array of generalist insect pollinators. Flower heads Plants develop the first leaves from the rhizome at the beginning are visited by Hymenoptera, Diptera, Lepidoptera and sporadically of spring and reproductive stems start to develop in June. A. amellus by Coleoptera (Landolt et al., 2010; Castro et al., 2011; Fig. 1c). is a late flowering species with long flowering period from mid- Among Hymenoptera, several species of Apidae (Apis sp., Ceratina July to September (Klotz et al., 2002), in some populations until sp., Epeolus sp., Xylocopa sp., and sometimes Bombus sp.), Megachil- mid-October. Diploid plants flower earlier than hexaploid plants idae (Heriades sp., Hoplosmia sp., and Megachile sp.), Halictidae (about one week earlier in the field) but there is a large overlap (Halictus sp.), Anthophoridae (Epeolus sp., Nomada sp.) and some- in flowering phenology (Castro et al., 2011). Fruiting period occurs times Formicidae have been observed. Diptera were also frequently in late summer from September to October. A. amellus has green observed, especially Syrphidae species (Eristalis sp., Episyrphus leaves in summer (Landolt et al., 2010). At the time of fruiting, new sp., Eupeodes sp., Helophilus sp., Scaeva sp. and Sphaerophoria sp.) side rosettes are formed at the dying flowering shoots (pers. obs.). (Vicidomini, 2006; Mayor, 2008; Castro et al., 2011). Several Lep- No specific data on factors responsible for initiation of flower- idoptera species belonging to different families have also been ing are available for A. amellus. Wallerstein et al. (2002), however, observed visiting the flower heads of A. amellus (e.g., Strymoni- showed for a garden cultivar Aster ‘Sun Karlo’ that flowering shoots dia sp., Lysandra coridon, Lycaenidae; Maniola jurtina, Aphantopus are initiated at day-length of 14 h, suggesting that this Aster species hyperantus, Nymphalidae; Pieris sp., Pieridae; Ochlodes venatus, is a long-day plant. This pattern could correspond to the type of Hesperioidea) (Loertscher et al., 1995; Castro et al., 2011). initiation of flowering of Aster amellus. It is in agreement with A survey of pollinator assemblage in several populations of observed phenology of A. amellus. diploid and hexaploid A. amellus in the Czech Republic revealed that pollinators are in general quite abundant. As a result, visitation rate Reproduction was high in all the studied populations (9–32 flower heads visited per 15 min). Usually insects visited 1–3 flower heads before switch- Flower heads ing to a different plant, promoting both self and cross-pollinations. The inflorescence is a capitulum (flower head) formed by sev- Pollinator assemblages strongly differ between populations. Obser- eral florets (Fig. 1b). Florets open gradually and centripetally. In vations of pollinator behaviour when facing diploid and hexaploid the hermaphrodite florets, the anthers are arranged in a tube and plants revealed that the most frequent pollinators have no prefer- pollen dehiscence occurs at the anthesis of each tubular flower, ence for a specific cytotype and thus disassortative pollen flow can with pollen being secondarily presented along the style as a result occur (Castro et al., 2011). of its growth through the anther tube. The stigma matures in subsequent days by the opening of the two-lobate stigmatic surface. Asexual reproduction including apomixis According to Lambers et al. (2008) Aster species require ver- Besides sexual reproduction, A. amellus is also able to reproduce nalization for initiation of flowering. Our personal experience with asexually by production of lateral ramets on a rhizome with sig- cultivation of the species in garden and greenhouse conditions sug- nificant impacts on population dynamics. The rhizome is 2–3 mm gests that vernalization is not a necessary condition for flowering, thick, lignified, and branched (Hegi, 1979). Clonal reproduction but transition through a cold period clearly increases the rate of is generally restricted to the close vicinity of the germination flowering. site (max. 5 cm; Mayor, 2008). According to CLO-PLA database (Klimesováˇ and de Bello, 2009), the plant can spread laterally Gamete development between 10 and 25 cm per year. The intensity of clonal reproduction Gamete development has been studied in detail for the diploid is the same in the two ploidy levels (Münzbergová, 2007a). A. amellus and several polyploid cultivars of Aster (Annen, 1945). The clonal growth organs are epigeogenous stems (rhizomes) The wild A. amellus had a normal development of both embryo sac and are considered as necessary for growth of the plant. The buds (monosporic polygonum type) and pollen grains, while the culti- resulting into the rhizomes are placed between 0 and 10 cm, below vars revealed high levels of sterility of male and female gametes due ground. During the vegetation season, the buds can also temporar- to degeneration of the cells occurring already before the meiosis ily occur up to 10 cm above ground. The rhizomes are frequently (Annen, 1945). rooting. New clonal ramets appear in a two-year cycle. The con- nection between the mother and daughter ramets persists for more Incompatibility system than two years. A mother plant usually creates only a single daugh- Species of the genus Aster generally possess a sporophytic ter ramet, even though two daughter ramets were also sometimes self-incompatibility system (Richards, 1986). However, partial self- observed (Schubert et al., 1987; Kutschera and Lichtenegger, 1992; compatibility may evolve in small populations of Aster species as Klimesováˇ and de Bello, 2009, pers. obs.). The rhizomes can be up a result of low diversity of S alleles (Giblin and Hamilton, 1999). to 7 years old (Landolt et al., 2010). The rhizomes serve also as stor- A. amellus has been previously described as a self-incompatible age organs, but the amount of reserves the plant is storing in these plant (Kovanda, 2005). Castro et al. (2011), however, demonstrated organs is quite limited (Landolt et al., 2010). that A. amellus is able to set seeds after self-pollination (in lower Apomixis is quite common in the Asteraceae family, for example amounts when compared with cross pollination), being partially in Hieracium and Taraxacum (Cichorioideae) and Antennaria (Aster- self-compatible. Self-pollination rates were not increased by mixed oideae), but has never been reported for A. amellus. Experimental loads of self and foreign pollen, i.e. pollen from a different cytotype, bagging of emasculated flower heads and the analysis of the ploidy indicating no mentor effect in A. amellus (this is due to the fact that levels of seeds confirm that autonomous apomixis does not occur A. amellus is self-compatible). However, seed germination after self- in A. amellus (Castro et al., 2011). The ability of pseudogamous pollination is lower than after cross pollination and the plant is thus apomixis still has to be investigated.

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Diaspores and dispersal mechanisms Herbivores and pathogens Based on the seed morphology (see section ‘Plant description’) A. amellus is described as a wind dispersed species (Landolt et al., Sorhagen (1881) reported that seeds of A. amellus are con- 2010). Terminal velocity of the seeds is 0.8 m/s indicating rela- sumed by a cutworm of Grapholitha tripoliana Barrett. (Lepidoptera, tively high potential to disperse by wind (Münzbergová, 2004) with Tortricidae, Eucosma tripoliana Barrett, according to current classi- no significant differences between the two ploidy levels. Without fication), which lives from August to beginning of October in the wind, with 0.8 m/s fall speed and 0.35 m capitulum height a mean seed cases of A. amellus. In October, the cutworm moves into the seed dispersion distance is about 0.44 m. With a 27 m/s wind speed, soil and metamorphoses after 8–9 months of dormancy. Similar seeds could reach up to 12 m (Tackenberg, 2001; Mayor, 2008). behaviour is characteristic for Coleophora obscenella Herrich- The seeds also have a good ability to attach to animal fur, with Schäffer (Lepidoptera: Coleophoridae). It is a monophagous moth, 79% of seeds staying on sheep fur for at least 10 min when attached. whose larvae feed on seeds of A. amellus (Baldizzone and Tabell, This suggests that the species has the potential to be transported 2002). Pupae develop in the ground and adults emerge in July and by exozoochory (Münzbergová, 2004). Pruchová˚ (unpubl.) also August (Vávra, 2004). Münzbergová (2006) showed that Coleophora showed that 81% of seeds are able to survive digestion by a mammal obscenella is common both in diploid and hexaploid populations in (using methodology of Kleyer et al., 2008) and there are no differ- the Czech Republic, with hexaploid plants suffering higher seed ences between diploid and hexaploid plants in this character. The damage than seeds of diploids. Mayor (2008) also recorded C. seeds thus have a potential to be dispersed also by endozoochory. obscenella in populations of A. amellus (diploid) in Switzerland. C. obscenella, can consume up to 95% of all seeds within a single flower head. Germination A potential seed feeder is also a fluorescent orange larva, from the cecidomyiid group of Diptera found in A. amellus populations A. amellus has a transient type of seed bank (Thompson et al., in Switzerland (Mayor, 2008) and in the Czech Republic (pers. 1997; Cerabolini et al., 2003; Czarnecka, 2004) with over 800 seeds obs.). From capitula of A. amellus collected in the Swiss populations, present in 1 m2 after seed shedding (Czarnecka, 2004). Despite the Mayor (2008) reared one individual of Euderus sp. (Hymenoptera, transient seed bank, seeds can be found up to 15 cm depth in quite Eulophidae), which parasitizes Lepidoptera larvae. high quantity (Czarnecka, 2004). Münzbergová (2004) showed that The vegetative parts of the plants are damaged by insect her- 42% of seeds remain viable in the seed bank over three years bivors, leaf miners, Orthoptera and Gastropoda (Mayor, 2008). when buried underground on a natural dry grassland locality. The Hering (1957) reports Liriomyza asteris Hg. and Phytomyza aster- same study, however, did not find delayed germination of seeds of ibia Hg. to be important miners on A. amellus. Larvae of an this species when sown on the soil surface. This suggests that the agromyzid fly Ophiomyia maura Meigen (syn. Agromyza maura, species has the potential to create a seed bank, but the seeds are not Melanagromyza maura; Agromyzidae, Diptera) mine in the stems dormant and germinate in the first year if the conditions are suit- of A. amellus (Barnes, 1937). Mammalian herbivores feed on capit- able (Münzbergová, 2004). In contrast, Raabová et al. (2007) found ula. Mayor (2008) also reports many fungal species (Ascomycota, higher number of established juveniles from sowing in the second Dothideomycetes) occurring on vegetative parts of A. amel- year of the experiment than in the first year, indicating that some lus (Ramularia, Cercospora, Phoma, Phyllosticta; determination seeds did not germinate until the second year. Similarly, Mayor by Adrien Boley according to Mayor, 2008). Marková (unpubl.) (2008) reports that seeds could stay in sites in dormant phase. recorded Puccinia asteris Duby (Basidiomycota, Urediniomycetes) Seeds usually germinate in spring (Czarnecka, 2004). Seed strat- on A. amellus in the Czech Republic. ification and scarification are not necessary for germination and Mayor (2008) indicates that intensity of biotic interactions is the seeds may rarely germinate also in autumn when there are higher at higher altitude and in less fragmented landscape. This is long warm autumn periods (Czarnecka, 2004). The seeds preferen- in agreement with findings of Münzbergová (2006) suggesting that tially germinate in small gaps, which can be partly shaded. They, seed herbivory is more intensive in larger populations of A. amellus. however, cannot germinate in full darkness, which is likely an adaptation to prevent germination in close sward (pers. obs.). Mycorrhiza

Response to competition and management A. amellus is dependent upon symbiosis with arbuscular mycorhizal fungi (AMF). Pánková et al. (2008) demonstrated that Competition has strong effect on performance of A. amellus.Ina diploid individuals of A. amellus from two regions in the Czech common garden experiment, the presence of Bromus erectus in the Republic do not survive for more than a few months without AMF. pots reduced growth and flowering of both diploid and hexaploid They have also demonstrated that plants from different localities plants (Münzbergová, 2007b). Similarly, competition with Calama- strongly differ in the degree of root colonization by AMF and that grostis epigejos and Tanacetum vulgare reduced survival and number the degree of root colonization is genetically based. Pánková et al., of shoots of A. amellus, especially when grown in nutrient rich con- 2011 also demonstrated that the plants grow the best when grown ditions (Kühn, 2006). In addition, flowering phenology of A. amellus in with AMF from their own localities in the soil from their own was delayed in localities with high productivity, i.e. with increased localities. This supports the conclusions of Raabová et al. (2007) competition (Castro et al., 2011). on existence of local adaptations in the species and extends it by A. amellus is a typical forest-fringe species in many areas. At knowledge on local adaptation to AMF. these habitats, it has obviously been favoured by cessation of pas- In a study comparing growth of A. amellus under different levels turing. It does not tolerate intensive grazing or mowing (Landolt of root colonisation by AMF, Pánková et al., 2011 demonstrated that et al., 2010). It, however, seems that it performs best during one there is a linear relationship between plant size and percentage or two decades after cessation of grazing and, after that period, it of root colonisation. This suggest that root colonisation by AMF decreases with the increasing spread of Brachypodium pinnatum or has a significant effect on plant growth over a wide range of root shrubs (Bobbink, 1987; Pautz et al., 1999). Therefore, the optimal colonisation. conservation management for this species corresponds to a low and Sudová et al. (2010) compared response to AMF between diploid irregular pasturing regime (Muller, 2002; Bernhardt et al., 2005). and hexaploid A. amellus from the Czech Republic. They have shown

Z. Münzbergová et al. / Perspectives in Plant Ecology, Evolution and Systematics xxx (2011) xxx–xxx 9 that while the diploid populations grow significantly better with dre” plants according to Walter (1931) with some transitions to AMF, the hexaploid plants grow equally well with and without “stenohydre” plants in its osmotic reaction (Müller-Stoll, 1935). mycorhizal symbiosis. In spite of this, AMF has strong significant A. amellus does not have physiological properties required for effect on amount of phosphorus in plant tissue in both ploidy levels. salt tolerance in contrast to Aster tripolium (Very et al., 1998; In a subsequent study growing diploid and hexaploid plant in their Kerstiens et al., 2002). In the halophyte A. tripolium, the stomata native soil and including also non-sterile soil treatment, Sudová closed in the presence of NaCI but opened in KCI, whereas the stom- et al. (unpubl.) demonstrated that both diploid and hexaploid ata of the glycophyte A. amellus opened to the same degree in both plants profit more from AMF fungi when grown in their native soil. NaCI and KCI (Very et al., 1998), as classically observed in other By cloning and sequencing, Sykorová´ et al. (unpubl.) detected more commonly studied non-halophytic species such as Commelina Glomus intraradices and Glomus badium (Glomeromycota, Glom- communis and Vicia faba (Pallaghy, 1970; Willmer and Mansfield, eromycetes) to be directly associated with roots of A. amellus in the 1969). A. amellus thus does not have an ability of induced stomatal field. closure in the presence of sodium ions in the apoplast surrounding the guard cells at high salinity (Kerstiens et al., 2002). Anatomy Biochemical data The stomata of A. amellus are developed on both sides of the leaves, but more stomata are found undersides than on the top, as No biochemical data on A. amellus are available. For biochemical usual also in other plant species in dry grassland communities (115 data on closely related species see below in section ‘Uses of the and 49 stomata per mm2, respectively; Müller-Stoll, 1935). species’. The presence of annual rings applicable for age determination was not studied in A. amellus. However, another species of the same Genetic data genus, Aster lanceolatus was found to create annual rings on woody rhizomes (Krivánek,ˇ 2003). The transition between the rings is, nev- Chromosome numbers ertheless, very variable and the rings are hardly visible (at least The basic chromosome number of Aster s. str. is x =9 (Funk 70× magnification is needed to see them). Krivánekˇ (2003) also et al., 2009; Cammareri et al., 2004). A. amellus agg. includes reported occasional occurrence of phloem pseudorings in the rhi- three cytotypes: diploids, tetraploids and hexaploids (Merxmüller zome making the identification of rings even more difficult. Also et al., 1976; see section ‘Taxonomy’). The only published record on other species from the family Asteraceae show variable or uncer- tetraploid cytotype comes from Fedorov (1969) from Russia indi- tain annual rings (Dietz and Ullmann, 1997). Based on our personal cating 2n = 36 for A. amelloides. Xiang and Semple (1996) report observations, similar structures can be recorded on the wooded existence of octoploid (2n = 72) cultivar of A. amellus from garden rhizomes of A. amellus. in Montreal (Quebec, Canada). Chromosome numbers that are not multiples of the basic chromosome count were reported for various Physiological data garden cultivars [2n = 66, counted in a plant of unknown origin in a Botanical garden in Freiburg (Huziwara, 1962); 2n = 66 and 2n =76 A. amellus occurs in habitats characterized by summer drought. in garden cultivars (Chatterjee, 1962); 2n = 66, 76, in cultivars of A. Soil temperature could reach 60–70 ◦C in summer and 40–60 ◦C amellus Goliath (Annen, 1945)]. at the cloudless days in spring (Müller-Stoll, 1935). Therefore, the species has physiological and morphological adaptations, such Molecular tools as root system, leaf structure and the number of stomata that Several molecular tools have been used with success to study enables it to survive during the dry periods (Müller-Stoll, 1935). A. amellus. Genetic diversity has been investigated using isozyme The numbers of stomata increase with increasing lack of water, markers (Raabová et al., 2007; Mandáková and Münzbergová, so plants occurring in dry habitats have usually high number of 2008). Furthermore, eight microsatellite markers have been stomata (Müller-Stoll, 1935). The leaves of A. amellus have no spe- described (Mayor and Naciri, 2007) and successfully used (Mayor, cific adaptations limiting transpiration. A. amellus has a tendency 2008). Recently, RAPD markers have been used to study distribu- to dormancy during the summer drought; the leaves fade and the tion of genetic diversity of A. amellus in Austria (Koch et al., unpubl.). plants do not flower in its usual flowering peak. However, most Nucleotide sequence data from the internal transcribed spacers of the plants are able to recover and to flower after the drought (ITS) of nuclear ribosomal DNA and amplified fragment length (Müller-Stoll, 1935). polymorphism markers (AFLP) have also been used successfully The yearly trend of osmotic values for A. amellus is related to to address phylogenetic relationships within Aster s.l., including A. the intensity of rainfall and soil humidity (Müller-Stoll, 1935). The amellus (Noyes and Rieseberg, 1999; Cammareri et al., 2004). Cas- osmotic values increase markedly in summer (15.6–21.7 atm) com- tro et al. (unpubl.) used sequences of the chloroplast atpI–atpH and pared to the values in spring (13–16 atm). Also, habitat conditions 5rps16-3trnK(UUU) intergenic spacers to analyze haplotype dis- affect the osmotic values so that they are higher in unprotected tribution and relationships between diploid and hexaploid plants areas (21.1 atm) than when protected under pine-trees (19.9 atm). in Central Europe. An enzymatic method for DNA extraction has Osmotic values increase also during the day; the increase from the been described and tested in 156 plant species, including A. amellus, morning until the afternoon is by 15.6–18.2%. The daily changes for which it was possible to obtain high-yield and high-molecular of osmotic values are closely related to the changes of plant water weight DNA (Manen et al., 2005). content (water deficit). Water deficit increases by 5.0–8.3% during the day and the total water deficit can reach up to 50% of water Distribution of genetic variation within and between populations content at saturation (Müller-Stoll, 1935). Similarly, transpiration Population genetic structure was investigated in 12 diploid and of A. amellus is restricted during the summer drought (Müller-Stoll, 9 hexaploid populations in the Czech Republic with isozyme mark- 1935). The stomata of A. amellus are very narrow or closed dur- ers (Mandáková and Münzbergová, 2008). Moreover, more detailed ing the drought (Müller-Stoll, 1935). Despite the stomatal closure, analyses were done for six of the 12 diploid populations in two water balance is stable only at the beginning of drought period. different regions in the Czech Republic (Raabová et al., 2007). Fur- These results suggest that A. amellus inclines to so called “euryhy- thermore, 31 diploid populations in Switzerland and France were

10 Z. Münzbergová et al. / Perspectives in Plant Ecology, Evolution and Systematics xxx (2011) xxx–xxx investigated using microsatellite markers (Mayor, 2008). Lastly, ous cauline leaves (Tzvelev, 2002). Hybrids between A. alpi- several populations of A. amellus were studied with RAPD mark- nus and A. amellus are also known as a garden cultivar ers along a 30 km stretch of the Danube Valley in Austria (Koch A. × alpellus hort. (web 2 http://www.bhg.com/gardening/plant- et al., unpubl.). dictionary/perennial/aster/ (accessed 05.12.2010)). In Ukraine, in Isozyme analysis revealed high genetic variation both within the vicinity of the cities of Chernogovka and Kiev, plants with and between populations (Mandáková and Münzbergová, 2008). smaller heads and narrower involucral bracts have been found, Analysis of molecular variance showed that most of the isozyme which are apparent hybrids between A. amellus L. s. l. and Erigeron variation was within populations (83.7%; FST = 0.16; p < 0.001), but acris L. s. l – × Asterigeron ucrainicus Tzvelev. sp. hybr. nova (Tzvelev, there was also significant variation among populations within a 2002). Garden hybrids are discussed in the section ‘Distribution in region (7.5%; FSC = 0.08; p < 0.001) (Raabová et al., 2007). Similarly, the secondary range and cultivation’. Koch et al. (unpubl.) found high molecular variation within populations (91%) and lower molecular variation among populations of Status of the species A. amellus (9%). Genetic differentiation (Fst) based on microsatellite markers increased with decreasing population size and with The species is considered critically endangered in Luxembourg decreasing density of surrounding populations (Mayor, 2008). In (web 3 http://www.mnhn.lu/recherche/redbook/vascplants/ contrast, there was no significant relationship between genetic default.htm (accessed 04.12.09)) and the Marche region in north- differentiation and geographic distance based on microsatellites ern Italy (not listed in the red list of the whole Italy, Conti et al., (Mayor, 2008), isozymes (Mandáková and Münzbergová, 2008) and 1992, 1997), regionally endangered in Austria (Adler et al., 1994; RAPD markers (Koch et al., unpubl.). However, there were some Fischer et al., 2008), endangered in the Czech Republic (Holub weak correlations at a small spatial scale (Raabová et al., 2007; and Procházka, 2000) and in several federal countries of Germany Mandáková and Münzbergová, 2008; Mayor, 2008). Overall, gene (Korneck et al., 1986; Frank et al., 1992; Buttler et al., 1997; flow within and between populations of A. amellus is negatively Scheuerer and Ahlmer, 2003) and least concern in Slovakia (web 4 affected by habitat fragmentation and small and isolated popula- http://ibot.sav.sk/checklist/ (accessed 04.12.09)). In Switzerland, tions of A. amellus experience a high genetic drift (Mayor, 2008). the species is currently declining (Landolt et al., 2010) and is Spatial distribution of genetic diversity within A. amellus pop- considered from vulnerable to least concern in different parts of ulations was studied in Switzerland using microsatellite markers the country (web 5 http://www.zdsf.ch/ (accessed 04.12.09)). The (Mayor, 2008). The general pattern of gene flow at the within- species is protected in France and is currently strongly declining all population level showed a significant positive structure below 30 m over the country (CBNBP-Délégation Centre, 2000). The species is (with higher structure below 2 m) and a significant negative struc- also declining in Poland, even though it is not protected (Zarzycki ture above 100 m. This structure can be explained by restricted et al., 2002). The species is not included in Natura 2000 (Council clonal propagation, limited dispersal abilities of this species as well of Europe, 1992), CITES (IUCN, 2004) or Bern Convention treaties as by more intense pollination events at low distances (Mayor, (Council of Europe, 2006). 2008). Within-population gene flow was positively influenced by an increasing density of individuals (Mayor, 2008). Comparison Uses of the species between discontinuous and continuous subpopulations showed that individual fragmentation had an impact on differentiation Local people in Azerbaidzhan use A. amellus (A. ibericus Stev.) between demes of individuals. After 50 m, a gap between individ- and other closely related Aster species (namely A. alpinus L. and uals allows a genetic differentiation process (Mayor, 2008). Gene A. tataricus L.) as medical plants (Mir-Babayev and Houghton, flow appears to be totally interrupted starting at 5 km of distance 2002). Aster tataricus contains two pentapeptides: asterin D and (Mayor, 2008). E(Cheng et al., 1996) and A. alpinus contains two clerodane deriva- tives related to salviarin and bacchotricuneatin A (Bohlmann et al., Heterozygosity, mean number of alleles and total allelic diversity 1985). The roots of A. tataricus are useful as an expectorant (Mir- The hexaploid plants had higher proportion of heterozygote Babayev and Houghton, 2002). According to Landolt et al. (2010) loci (66.23%) than the diploid plants (37.55%) (Mandáková and A. amellus is edible and was used by local people in the past in Münzbergová, 2008). Based on isozyme markers, mean allelic rich- Switzerland. No uses are, however, reported from Switzerland ness per population ranged from 2.531 to 3.135 (mean = 2.767), today. A. amellus is a very decorative plant and provides source gene diversity from 0.375 to 0.560 (mean = 0.487) and inbreed- for selection of new forms (Tamamshyan, 1990), see section ‘Dis- ing coefficient from −0.212 to 0.459 (mean = 0.071) (Raabová tribution in the secondary range and cultivation’. et al., 2007). The microsatellite markers provided much higher genetic diversity. The number of alleles ranged between 4 and Acknowledgements 30 (mean number of effective alleles = 5.8; Mayor, 2008). The We thank J. Chrtek for help with the synonyms, E. Welk mean gene diversity ranged from 0.419 to 0.957 (mean = 0.744; for providing the map and information about species distribu- Mayor, 2008). Three loci displayed significant heterozygote defi- tion and its limits, D. Pruchová˚ and Z. Sykorová´ for providing ciencies, which might indicate the presence of null alleles (Mayor, their unpublished data, M. Chytry´ for advice when unifying the 2008). Both mean observed heterozygosity (R2 = 0.36, p < 0.001) and syntaxonomical units, T. Dostálek, R. Rosenbaumová and E.J. mean gene diversity (R2 = 0.63, p < 0.001) increased with population Jäger for valuable comments on the manuscript. ZM was sup- size. Moreover, both heterozygosity and gene diversity positively ported by GACRˇ 526/09/0549 and institutional research grants influenced germination rate. This indicates a risk of inbreeding MSM 0021620828 and AV0Z60050516. JR was supported by depression in small populations of A. amellus (Mayor, 2008). MK00002327201 and GACRˇ P505/11/P482. SC was supported by FCT grant BPD/41200/2007 and GACRˇ grant P506/10/P188. Hybrids

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