Polyploidy and Karyotype Variation in Turkish Bellevalia (Hyacinthaceae)

Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2003? 2003 143? 8798 Original Article

CYTOLOGY OF TURKISH BELLEVALIA M. A. T. JOHNSON Botanical Journal of the Linnean Society, 2003, 143, 87–98. With 13 figures

Polyploidy and karyotype variation in Turkish Bellevalia (Hyacinthaceae)

MARGARET A. T. JOHNSON*

Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019

Received February 2003; accepted for publication June 2003

There are 20 Bellevalia species in Turkey, half of which are endemic. Chromosome numbers are known for 15 species. A chromosome survey of 145 Bellevalia individuals showed that the karyotype is remarkably stable. All are based on x = 4. The majority are diploid with 2n = 8, but there is also a polyploid series of 2n = 16, 24 and 32. Aneuploidy occurs only at the octoploid level. Eleven individuals had metacentric B chromosomes, one had acrocentric Bs and one had telocentric Bs. Bellevalia pycnantha and B. paradoxa are morphologically similar, with B. pycnantha reduced to a synonom of B. paradoxa.© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 87–98.

ADDITIONAL KEYWORDS: aneuploid – B chromosome – chromosome number – endemic – morphology – synonymy – taxonomy.

INTRODUCTION Johnson (1994) and by Özhatay, Johnson & Mathew (1991a) as 2n = 8 and 24, respectively. A further 42 of The genus Bellevalia (Hyacinthaceae) comprises the counts given here were included in a list of counts spring-flowering bulbous plants which occur mostly in lacking locality data by Johnson & Brandham (1997). the mediterranean and central Asia area. The World These are indicated on Table 1. Checklist of Seed Plants (Govaerts, 1996) gives 74 species of Bellevalia, although four species, B. acutifolia, B. anatolica, B. forniculata and B. paradoxa are omit- DISTRIBUTION ted. In the Flora of Turkey & the East Aegean Islands, Although the genus occurs throughout much of Ana- Wendelbo (1984) listed 18 species from Turkey, seven tolia and European Turkey, many species are very of which are endemic. Later, Wendelbo (1985) reduced localized. Three, B. trifoliata, B. sarmatica and the B. latifolia to a synonym of B. olivieri. The second sup- recently described B. edirnensis (Özhatay et al., plement to the Flora, Volume 11 (Güner et al., 2000), 1991a) have been recorded only in European Turkey. added three more species; B. mathewii Özhatay & Bellevalia paradoxa s.l. occurs only in eastern areas Koçak, B. anatolica B. Mathew & Özhatay and where it favours moist boggy habitats. Also found only B. edirnensis Özhatay & B. Mathew. Following the in the east, to the south of Lake Van, is B. longistyla. reduction of B. pycnantha to a synonym of Bellevalia trifoliata grows in the south and western B. paradoxa, as given below, there are 19 Turkish spe- coastal regions within the Mediterranean floristic cies, nine of which are endemic. areas, and B. clusiana occurs in central Anatolia. Bell- A cytological investigation of 145 individuals in 15 evalia modesta is found in the Taurus mountains Turkish Bellevalia species was undertaken at the above Adana. Royal Botanic Gardens, Kew to survey chromosome Some species are restricted to a few areas. For numbers and variation within populations. Two spe- example, B. forniculata grows in great numbers along cies, B. anatolica and B. edirnensis, were counted by the Çat roadside in flat damp grassland areas at the foot of the Palandöken mountains. Growing alongside it is the closely related genus Muscari, *E-mail: [email protected] M. armeniacum or M. aucheri. Large populations of

88 M. A. T. JOHNSON

Table 1. Localities and chromosome numbers of the 145 individuals studied

Kew accession Cytology Locality, collector, voucher no. reference 2n

B. anatolica 1 plant B7 ELAZIGˇ : N of Elazigˇ nr Pertek on Tunceli rd. 1987 -1964 87.453 ‡ 8 Rocky hillside. B. Mathew, K & Photo

B. clusiana 2 plants A4 ANKARA: Kızılcahamam to Çerkes¸ . 16 km from Çerkes¸ . 1984–3629 84.590 § 8 1250 m. In ﬁelds. N. & E. Özhatay, ISTE 54116 K & Photo 1992–2340 84.591 8 Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019

B. edirnensis 2 plants A1(E) EDI˙ RNE: Edirne to Uzunköprü. 1 km from I˙ brik tepe rd none none 24 junction. 250 m. Fields & meadows. ISTE 59752, B. Mathew, none 93–14*† 24 K & EDTÜ & Photo

B. fominii 4 plants A7 GÜMÜS¸ HANE: 20 km SE Gümüs¸ hane on Bayburt rd. 1700 m. 1985–2129 85.154 * 8 Cultivated ﬁeld by stream. M. A. T. Johnson 169, K & Photo 1992–2468 85.155 § C10 HAKKARI˙ : Between Yüksekova and S¸ emdinli J. C. 1985–4235 85.908 8 Archibald 6577, K & Photos 1992–2341 85.909 § 8, n = 4 B. forniculata 38 plants B8 ERZURUM: Foot of Palandöken Mts. 22 km S of Erzurum on 1982 -2985 82.929 § 8 Çat rd. 2000 m. Wet & dried out areas open meadows. M. A. T. 1985–2147 85.228 8 Johnson 92 K & Photo 1992–2345 85.229 8 B8 ERZURUM: Foot of Palandöken Mts. 28 km SW of Erzurum on 1985–2346 85.230 8 Çat rd. 2000 m. Wet meadows. M. A. T. Johnson 187, K & Photo 1992–2347 85.231 8 1992–2349 85.233 8 1992–2350 85.234 8 1992–2351 85.235 8 1992–2352 85.236 8 As above. (white form) M. A. T. Johnson 188, K & Photo 1985–2148 85.237 § 8 As above. M. A. T. Johnson 189, K 1992–3197 85.239 8 1992–3199 85.240 § 8 1992–2149 85.242 8 As above. M. A. T. Johnson 190 1992–2353 85.244 8 1992–2354 85.245 8 1992–2355 85.246 8 As above. M. A. T. Johnson 191A, K 1985–2151 85.249 § 8 1992–2358 85.250 8 1992–2359 85.251 8 1992–2360 85.252 8 1992 -1041 85.253 8 1992–2362 85.254 8 As above. M. A. T. Johnson 191B 1985–2152 85.255 8 1992–2363 85.256 8 1992–2364 85.257 8 As above. (White perianth edges) M. A. T. Johnson 192 1985–2153 85–259 § 8 As above. (Albino form with white ﬂowers.) M. A. T. Johnson 193 1985–2154 85.260 8, n = 4 A9 KARS: 4 km SW of Sarıkamıs¸ . Yeniköy and Horasan rd. 2250 m. 1985–2182 85.375 8 Wet meadows. M. A. T. Johnson 221 A 1992–2367 85.376 8 1992–2368 85.377 8 1992–2369 85.378 8 1992–0655 85.379 8 1985–2183 85.382 8

CYTOLOGY OF TURKISH BELLEVALIA 89

Table 1. Continued

Kew accession Cytology Locality, collector, voucher no. reference 2n

1992–2373 85.383 8 As above M. A. T. Johnson 221B, K 1992–2374 85.284 8 1992–2375 85.385 8 1992–2376 85.386 8 B8 KARS: 30 km from Erzurum on Çat rd. T. Baytop, ISTE 41976 none 85.83 § 8

B. gracilis 1 plant Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 A6 TOKAT: Çamlıbel. J. C. Archibald 7569, K 1987 -2008 86.1383 § 8 + 3 meta Bs

B. kurdistanica 1 plant C10 HAKKARI˙ : Zap Gorge nr Bagˇ ıs¸ lı 1500m. J. C. Archibald, K 1986–6230 94.76 § 8

B. longistyla 26 plants B9 VAN: 8 km S on Gürpınar rd. 1850 m. Below radio station. Dry 1985–2227 85.507 32 cultivated field. M. A. T. Johnson 263, K & Photos 1992–2377 85.508 § 32 1992–2378 85.509 32 1992–2379 85.510 32 1992–2380 85.511 32 1992–2381 85.512 32, n = 16 1992–2382 85.513 32 1992–2383 85.514 32 1992–2377 85.508 § 32 1992–2378 85.509 32 1992–2379 85.510 32 1992–2380 85.511 32 1992–2381 85.512 32, n = 16 1992–2382 85.513 32 1992–2383 85.514 32 B9 VAN: Artos mts. 24 km N of Çatak on minor rd to Van. 2600 m. 1985–2257 85.575 § 30 + telo fragment Rocky mt slopes near snow patches. M. A. T. Johnson 288, K As above. 2200 m. M. A. T. Johnson 295, K & Photo 1985–2264 85.581 32 1992–2440 85.582 31 + 1 meta B & telo fragment 1992–3722 85.583 32 + 1 meta B 1992–2441 85.584 32 1992–2442 85.585 § As above. M. A. T. Johnson 301, K 1992–2443 85.615 § 32 1992–2444 85.616 * 32 As above. M. A. T. Johnson 302, Photo 1985–2272 85.617 32 B9 VAN: 85 km W of Van on Bitlis rd. 2200 m. Highest point on rd 1985–2279 85.637 § 35 over pass. Open mt top. M. A. T. Johnson 310, K & Photo B9 VAN: no further data. M. A. T. Johnson 319, K 1985–2288 85.676 § 32 B9 VAN: SW of Van, above Edremiet, 1700 m. J. C. Archibald 6303, 1985–4231 85.900 32 K, E & Photo 1994–0383 94.10 32 B9 VAN: Erçek. J. C. Archibald 6629, K & Photo 1985–4230 85.898 32 1992–2384 85.899 § 32 B9 VAN: Artos dagˇ . Catak D. Foreman none 85–929 33 none 85–930 31 none 85–931 33 B. modesta 2 plants C4 I˙ ÇEL: 17km E of Mut on Kırobası rd. 1300m. Cornfield by 1990–2207 90.328 8 roadside. Johnson, Cowley & Doherty 73/90–337, K C4 I˙ ÇEL: 3km E of mut. 400m . Hills. In fields. M. Koyuncu 1984–991 84.156 § 8 4782, K & Photos

Table 1. Continued

Kew accession Cytology Locality, collector, voucher no. reference 2n

B. paradoxa 19 plants B8 ERZURUM: 22 km S Erzurum on Çat rd. 2000 m. Wet and dried 1982 -2992 82.948 § 8 out areas in open meadows. M. A. T. Johnson 99, K & Photo A10 KARS: 14 km SW Sarıkamıs¸ . M. A. T. Johnson 116 1982–3000 82.1001§ 8 B9 VAN: 82 km SE of Van on Bas¸ kale rd. Top of Çuh Pass. 2800 m. 1985–2245 85.541§ 8 Exposed mountain slopes amongst rocks & grassland. M. A. T. 1985–2245 84.542 8 Johnson 277, K 1985–2245 84.543 8 Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 1985–2245 84.544 8 1985–2245 84.545 8 1985–2245 84.550 8 1985–2245 84.551 8 B9 VAN: Artos mts. 24 km N of Çatak on minor rd. Rocky mt slopes, 1985–2245 84.552 8 snow patches. M. A. T. Johnson 300, K 1985–2269 85.604 8 1992–2425 85.605 § 8 1992–2426 85.606 8 + 3 telo Bs 1992–2427 85.607 8 1992–2428 85.608 8 1992–2429 85.609 8 1992–2430 85.611 8 1992–3719 85.612 8 B/C9 Bahçesaray. J. C. Archibald 7604, Photo 1987-2009 86.1384 § 8 B. paradoxa (as B. pycnantha) 23 plants A10 KARS: 17 km N of Karakurt. LH side of rd going up Sarıkamıs¸ 1982–3000 82.966 § 16 Pass. 2000 m. Dry rocks. M. A. T. Johnson 107, K As above RH side of rd going up Sarıkamıs¸ Pass 2000 m. Damp 982–3003 82.982 § 16 areas by stream. M. A. T. Johnson 110, K & Photo A9 KARS: 4 km W of Sarıkamıs¸ Yeniköy to Horasan rd. 2250 m. Wet 1992–2407 85.324 § 16 meadows. M. A. T. Johnson 208, K A9 KARS: 10 km from Sarıkamıs¸ Along old pass rd. 220 m. Pinus 1992–2170 85.325 § 16, n = 8 sylvestris forest. Wet meadows by stream. M. A. T. Johnson 210, K 1992–2408 85.326 16 & Photo 1992–2409 85.327 16 1992–3717 85.328 § 16 A9 KARS: 4 km W of Sarıkamıs¸ . Yeniköy to Horasan rd. 2250 m. Wet 1985–2174 85.336 § 16 + 2 acro Bs meadows. M. A. T. Johnson, 214, K & Photo 1992–2412 85.339 16 1992–2413 85.340 16 1992–2414 85.341 § 16, n = 8 A9 KARS: 4 km W of Sarıkamıs¸ . Yeniköy to Horasan rd. 2250 m. Wet 1992–2416 85.348 16 meadows. M. A. T. Johnson 216 A, K 1992–2417 85.349 § 16 1992.2418 85.350 16 B9 AGˇ RI: New Horasan to Agˇ rı rd. Through village of 1985–2177 85.351 16 Tahir. 2400m. M. A. T. Johnson 216B, K 1999–2419 85.352 § 16 1999–2420 85.353 16 1999–2421 85.354 * 16 1992–2422 85.355 16, n = 8 B9 AGˇ RI: New Horasan to Agˇ rı rd. Through village of 1985–2184 85.387 § 16, n = 8 Tahir. 2400m. M. A. T. Johnson 222 A, K 1992–2423 85.388 16 B9 AGˇ RI: Tutak. J. C. Archibald 6338, K & Photo 1987 -2007 86.1591 16 B9 VAN: Çuh Pass. 3000m. Marshy areas with running snowmelt. 1994–384 94.11 16 J. C. Archibald 6530, E & Photo

Table 1. Continued

Kew accession Cytology Locality, collector, voucher no. reference 2n

B. rixii 9 plants B9 VAN: 82 km SE Van on Bas¸ kale rd. Top of Çuh Pass. 2800 m in 1985–2252 85.564 8 dry rocks. M. A. T Johnson 283, Photos, Type locality 1992–2435 85.565 8 1992–2436 85.566 8 1992–2437 85.567 8 1992–2438 85.568 8 Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 1992–2439 85.569 8 B9 VAN: 82 km SE Van on Bas¸ kale rd. Top of Çuh Pass. 2800 m. 1992–2432 85.520 8 Exposed mt slopes rocks and grassland. M. A. T. Johnson 269, Type 1992–2433 85.521 8 locality 1992–2434 85.522 8 B. sarmatica 11 plants B9 AGˇ RI: 45km S Agˇ ri on Ercis¸ rd. 1700m Cultivated fields 1985–2220 85.485 § 8 by roadside. M. A. T. Johnson 256, K & Photo B5 KAYSERI: 28 km E of Kayseri on Bünyan rd. 1150 m. Open 1990 -2037 90.162 8 + 3 meta Bs rocky slopes & wet muddy places by stream. Edge of fields nr drinking water fountain. Johnson, Cowley & Doherty 3/90–7 As above. Johnson, Cowley & Doherty 3/90–10, Photo 1990–0241 90.165 8 + 4 meta Bs A6 TOKAT/SI˙ VAS: Çamlıbel-Yıldizelı. Çamlıbel Pass. 1650 m. ISTE 1984–3628 84.588 § 8 54525 1984–3628 84.589 8 + 4 meta Bs B9 AGˇ RI: Above Eles¸ kirt. J. C. Archibald 6370, K 1995–4234 85.906 8 1992–2447 85.907 § 8 A6 TOKAT: Çamlıbel. J. C. Archibald 6950, K 1985–4233 85.903 8 + 3 meta Bs & dicentric n = 4 1992–2445 85.904 8 + 0–3 meta Bs 1992–2446 85.905 §* 8 + 2 meta Bs B9 AGˇ RI: Just S of Agˇ ri. Roadside bank & fields. Heavy soil. 1987 -1955 87.442 8 B. Mathew 11011 B. tauri 2 plants C3 ANTALYA: SW of Antalya. Çalbalı dagˇ . Above Saklıkent village 1988–2731 88.124 § 8 M. A. T. Johnson 497, K & Photo C3 ANTALYA: Tahtalı dagˇ above Kemer nr Ovacik village. 1030m. 1988–2741 88.132 § 16 Alpine meadow. M. A. T. Johnson 510, K & Photo B. trifoliata 3 plants A2(A) I˙ STANBUL: Yalova to Termal rd. 5 km E of Yalova. Karaca 1987– 1748 87.357 § 8 Arboretum. Fruit orchard. M. A. T. Johnson 357, K 1992–3567 92.132 8 A3 BOLU: Abant Lake, SE of Bolu, picnic area. 1250 m. Open rocky 1987– 1784 87.424 § 8 slope above lake nr rd. Among Juniperus communis ssp. nana. M. A. T. Johnson 392B, K

* Chromosome number, somatic cell and karyotype published in Özhatay et al. (1991a). † Chromosome number, somatic cell and karyotype published in Özhatay et al. (1991b). ‡ Chromosome number, somatic cell and karyotype published in Johnson (1994). § Chromosome number published in Johnson & Brandham (1997).

B. paradoxa also occur, but more frequently only a species. Wendelbo (1980) listed 20 more species, few plants or even just one solitary individual are including three new Turkish species, B. crassa, B. rixii seen. and B. modesta. The list also added four other Turkish species, B. forniculata, B. paradoxa (Fig. 1), B. pycnantha and B. tristis, which Feinbrun (1938–9) TAXONOMY had omitted from her monograph. Feinbrun (1938–39) published a comprehensive study There are few good morphological differences of the genus, which at that time comprised about 50 between Bellevalia and some other genera, leading to

© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 87–98 92 M. A. T. JOHNSON misidentification not only with its closest ally, Mus- 1988) provided an index of chromosome counts, giving cari, but also with Hyacinthus (Wendelbo, 1980) and numbers for six Turkish species, five by Von Bothmer Strangweja (Persson & Wendelbo, 1979). In Bellevalia, & Wendelbo (1981) and one by Wendelbo (1984). It also the free parts of the six filaments (which are of equal included a count of 2n = 8 for B. trifoliata from the length and fused with the perianth tube for more or East Aegean island of Rhodos by Von Bothmer & less their whole length), are more or less triangular, Bentzer (1973). Volume 11 included another index of flat and usually connate at the base (Persson & Wen- counts by Özhatay, Sadıkogˇ lu & Johnson (2000), delbo, 1979). This is unlike its closest relative, Mus- which gave 49 counts for 17 species (including 11 new cari, with which it frequently confused, where the six species not included in Volume 10) by Özhatay et al., anthers are of two distinct lengths; three long and 1991a, b), Johnson (1994), Mirici & Arslan (1994), three short. Özhatay & Johnson (1996), Dalgiç & Bas¸ ak, 1996), Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 Some Bellevalia species are very similar, with few Johnson & Brandham (1997) and Dane (1999). These distinguishing characters, making identification diffi- are given in Table 2. cult especially from herbarium specimens unless bud Chromosome data are now available for all but and flower colour are noted before pressing. four species; B. crassa, which is known only from B. sarmatica and B. gracilis both have similar rather the type collection from Erzincan, Refahiye; the unattractive lax muddy-coloured inflorescences with once-collected B. latifolia from Hakkari in south-east long pedicels. Other species, such as B. forniculata Anatolia; B. longipes which has been recorded with its unusual electric blue flowers, are easily dis- mainly from east Anatolia (Mesopotamia) and the tinguishable in the field. B. paradoxa has compact, recently discovered B. mathewii from the moun- attractive darkish blue inflorescences and tains above Alanya. B. edirnensis has longer inflorescences bearing cream This paper summarizes the Turkish chromosome to pale yellow or greenish violet flowers. data on the genus to date, gives 103 new counts and In cultivation morphology may change considerably. reduces B. pycnantha into the closely allied species, For example the leaves of B. modesta in the wild are B. paradoxa. reflexed, but in cultivation at the Royal Botanic Gar- dens (RBG), Kew they are erect. MATERIAL AND METHODS Most of the bulbs were collected between 1982 and CYTOLOGY 1990 and were cultivated in the Living Collections The first supplement of the Flora of Turkey and the Department at the Royal Botanic Gardens, Kew. East Aegean Islands, Volume 10 (Davis, Mill & Tan, Locality data and donors’ collection details are given in Table 1. Root-tips were sampled from each bulb, which was separated or individually potted. Chromo- some counts were obtained from root-tips using a stan- dard Feulgen squash method as given in Johnson & Güner (2002). Meiotic studies for seven plants were prepared by squashing fresh anthers in a drop of 2% acetic-orcein. All slides were made permanent with

CO2 under pressure (Bowen, 1956) and are retained in the Jodrell Laboratory. Somatic cells were photo- graphed on a Zeiss Photomicroscope III using PAN F ﬁlm. Table 1 lists herbarium vouchers made in the ﬁeld (ISTE), or taken from cultivated plants at RBG, Kew (K) and plant reference slides taken both in habitat and/or in cultivation (Photo).

RESULTS

CYTOLOGY Chromosome counts and ploidy levels All the 145 individuals listed in Table 1 had chromo- Figure 1. Two cultivated inﬂorescences of Bellevalia par- some numbers based on x = 4. The majority, 93 counts, adoxa. Left: diploid Johnson 99 (82–948). Right: tetraploid were diploid with 2n = 8 and no karyotype differences Johnson 214 (85–339). could be detected between the species. Figures 2, 3, 6

Table 2. Published chromosome counts for Turkish Bellevalia species

Species 2n = Reference

*B. anatolica B. Mathew & Özhatay 8 Johnson (1994) *B. clusiana Griseb. 8 Von Bothmer & Wendelbo (1981) 8 Özhatay et al. (1991a) 8 Mirici & Arslan (1994) 8Johnson & Brandham (1997) *B. crassa Wendelbo unknown B. dubia (Guss.) Roem. & Schult. unknown

*B. edirnensis Özhatay & B. Mathew 24 Özhatay et al. (1991a) Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 24 Özhatay et al. (1991b) 24 Johnson & Brandham (1997) 24 Dane (1999) B. forminii Woronow 8 Özhatay et al. (1991a) 8Johnson & Brandham (1997) *B. forniculata (Fomin) L.N. Delaunay 8 Wendelbo (1984) 8 Özhatay et al. (1991a) 8Johnson & Brandham (1997) *B. gracilis Feinbrun 8 + 0–3 meta Bs Özhatay et al. (1991a) 16 Mirici & Arslan (1994) 8 + 3 meta Bs Johnson & Brandham (1997) B. kurdistanica Feinbrun 16 Von Bothmer & Wendelbo (1981) 8Johnson & Brandham (1997) B. longipes Post unknown B. longistyla (Miscz.) Grossh. 32, 33, 35 Özhatay et al. (1991a) 31, 32, 35 Johnson & Brandham (1997) B. macrobotrys Boiss. unknown *B. mathewii Özhatay & Koçak unknown *B. modesta Wendelbo 8 Özhatay et al. (1991a) 8 Mirici & Arslan (1994) 8Johnson & Brandham (1997) B. oliveri (Baker) Wendelbo (as B. latifolia Feinbrun) 32 Özhatay et al. (1991a) B. paradoxa (Fisch. & C.A. Mey.) Boiss. 8 Özhatay et al. (1991a) 8 Özhatay & Johnson (1996) 8Johnson & Brandham (1997) as B. pycnantha (K.Koch) Losinsk. 8, 8 + 3 telo Bs Özhatay et al. (1991a) 16, 16 + 2 telo Bs (as B. pycnantha/B. paradoxa)8Johnson & Brandham (1997) *B. rixii Wendelbo 8 Özhatay et al. (1991a) 8 Özhatay & Johnson (1996) B. sarmatica (Pall.) Woronow 8 Özhatay et al. (1991a) (as B. sarmatica/longistyla) 8 + 0–3 meta Bs Von Bothmer & Wendelbo (1981) 32, 32 + BJohnson & Brandham (1997) *B. tauri Feinbrun 8, 16 Von Bothmer & Wendelbo (1981) (as B. dubia)8Özhatay et al. (1991a) 8Johnson & Brandham (1997) 16 Johnson & Brandham (1997) B. trifoliata (Ten.) Kunth 8 Von Bothmer & Wendelbo (1981) 8 Özhatay et al. (1991a) 8 Dalgiç & Bas¸ ak 1996) 8Johnson & Brandham (1997)

* = endemic species and 11 show somatic cells of B. clusiana (84–591); ploidy). Of the two counts for B. tauri from individual B. forniculata (85–383); B. modesta (84–156) and B. plants from different localities, 88–124 was diploid trifoliata (87–357), all with a typical diploid karyotype (Fig. 12A) and 88–132 was tetraploid (Fig. 12B). Of of one pair of sub-metacentrics, one pair of acrocen- the 42 plants of B. paradoxa, 19 were diploid and 23 trics and two pairs of smaller sub-metacentrics. There were tetraploid. Both hexaploid counts were for were 24 tetraploid counts (2n = 16), two hexaploids B. edirnensis and all the octoploid counts were for (2n = 24) and 26 octoploids (2n = 32, with some aneu- B. longistyla.

Meiotic studies in seven diploid individuals con- tric. The diploid, 85–606, had three telocentric Bs ﬁrmed the somatic counts and showed regular chro- (Fig. 12C) and the tetraploid individual, 85–336, had mosome pairing. Figure 13 shows four bivalents in two acrocentric Bs (Fig. 12D). B. sarmatica (85–485). Aneuploidy B chromosomes Aneuploidy was found among the 26 individuals stud- Of the 145 plants studied, 13 individuals were found ied in the single octoploid species B. longistyla. Most to have B chromosomes. Nine of these were diploids, were euploid with 2n = 32. Six were aneuploid, with one was a tetraploid and three were octoploids. The 2n = 30 (85–575); 2n = 31 (85–582 and 85–930); number of Bs ranged from one to four, with three the 2n = 33 (85–929 and 85–931, Fig. 4); and 2n = 35 (85– most common (Figs 7–10, 12C, D). B chromosomes 637, Fig. 5). Additionally, 85–575 and 85–582 had telo- Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 were usually metacentric, but in two individuals of centric fragments and a metacentric B chromosome B. paradoxa they were either telocentric or acrocen- was seen in three plants, 85–582, 82–583 and 85–585.

10 *

78 911

Figures 2–11. Somatic chromosomes of Bellevalia species. Scale bar = 5 mm. Fig. 2. B. clusiana (84–591), 2n = 8. Fig. 3. B. forniculata (85–383), 2n = 8, 2 satellites arrowed. Fig. 4. B. longistyla (85–931), 2n = 33. Fig. 5. B. longistyla 2n = 35 (85– 637). Fig. 6. B. modesta (84–156), 2n = 8. Fig. 7. B. sarmatica (85–903), 2n = 8 + 3 metacentric Bs with dicentric arrowed. Fig. 8. B. sarmatica (85–903), 2n = 8 + 3 metacentric Bs, with unstable dicentric chromosome (arrowed) and fragment asterisked. Fig. 9. B. sarmatica (85–903), 2n = 9 + 3 metacentric Bs with telocentric fragment (arrowed). Fig. 10. B. sarmatica (85–903), 2n = 8 + 3 metacentric Bs with no dicentric. Fig. 11. B. trifoliata (87–357), 2n = 8. Satellite arrowed.

B Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019

C Figure 13. Meiotic chromosomes of Bellevalia sarmatica (85–485), with 4 bivalents. Scale bar = 5 mm.

TAXONOMY

D Figure 1 shows the inﬂorescences of two cultivated plants of B. paradoxa. The diploid plant 82–948, shown left, is a more violet/magenta shade of blue than the tetraploid 85–339, shown right, but other- wise they are virtually indistinguishable. In habitat the larger more vigorous tetraploid plants have a wider distribution in wet boggy meadows than the more diminutive diploid plants, which grow only at higher altitudes in generally drier, rocky habitats or alpine pastures. However, this size difference is lost in cultivation. B. pycnantha is here reduced to a syn- Figure 12. Karyotypes. A, Bellevalia tauri (88–124) onym of B. paradoxa which is the older name. 2n 8. B, B. tauri (88–132) 2n 16. C, B. paradoxa (85– = = Bellevalia paradoxa (Fisch. & C. A. Mey.) Boiss., Flora 606) 2n = 8 + 3 telocentric Bs. D, B. paradoxa (85–336) Orientalis 5: 368 (1882). 2n = 16 + 2 acrocentric Bs. Scale bar = 5 mm. Basionym: Hyacinthus paradoxus Fisch. & C. A. Mey. in Index Seminum Hortus Petropolitanus 1: 30 (1835). Synonyms: Muscari paradoxum (Fisch. & C. A. Mey.) K. Koch in Linnaea 22: 253 (1849). Chromosomal aberrations Bellevalia pycnantha (K. Koch) Losinsk., Flora URSS One diploid individual of B. sarmatica (85–903), in 4 : 404 (1935). New synonym. addition to having three metacentric B chromosomes, Muscari pycnanthum K. Koch in Linnaea 22: 255 sometimes had an unstable dicentric chromosome (1849). where a number of abnormal chromosome products were observed. Figures 7 and 8 show the dicentric DISCUSSION chromosomes arrowed with an additional fragment asterisked in Figure 8. The somatic cell in Figure 9 Chromosome studies are a useful taxonomic tool to with 2n = 9 + 3B has no dicentric chromosome but has identify Bellevalia species at the generic level, as the a telocentric fragment arrowed. genus is easily distinguished by its large chromosomes

© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 87–98 96 M. A. T. JOHNSON based on x = 4. The typical karyotypes of related gen- in polyploids, as for example in Aloe elgonica era Muscari (2n = 18), Pseudomuscari (2n = 18), Hya- (Brandham & Johnson, 1977), where because of the cinthus (2n = 16) and Hyacinthella (2n = 18) were presence of several other complete sets of chromo- illustrated by Garbari (1981). somes, an imbalance of chromosome number can be tolerated. The aneuploids in Bellevalia found here are simply loss or gain of normal chromosomes. There is POLYPLOIDY no evidence that it is the result of chromosome fission Apart from the tetraploid counts for B. gracilis by or fusion. Mirici & Arslan (1994) and B. kurdistanica by Von The karyotypes shown here of B. tauri, 2n = 16 Bothmer & Wendelbo (1981), all previously published (Fig. 12B) and B. paradoxa (Fig. 12D), together with counts shown in Table 2 agree with the results in those of octploid B. longistyla (fig. 3C in Özhatay et al., Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 Table 1. The material of B. gracilis (86–1383), studied 1991a) and hexaploid B. edirnensis (fig. 4B in Özhatay here from north-west of Sivas, had 2n = 8 + 0–3B, et al., 1991b), show that the sets of chromosomes in although Mirici & Arslan (1994) reported that their these polyploids are similar within each set. This sug- material, which they identified as the same species, gests that it is more likely that the polyploidy has from east of Sivas was tetraploid, 2n = 16. Von Both- arisen as autoploidy rather than alloploidy. This view mer & Wendelbo (1981) found that their material of agrees with that of Von Bothmer & Wendelbo (1981), B. kurdistanica was tetraploid, although the material although Feinbrun (1938–39) had suggested that poly- studied here, also collected from the Zap gorge, ploidy within the genus is of allopolyploid origin. Hakkari, was diploid. In the two collections of B. tauri from different mountains west of Antalya, one was diploid (88–124) and the other tetraploid B CHROMOSOMES (88–132). From the 45 collections studied by Von Bothmer & For material identified as B. paradoxa, 19 plants Wendelbo (1981), metacentric B chromosomes were were diploid and 23 were tetraploid. The plants in all found in just two plants of Iranian material of the localities were chromosomally uniform, except for B. saviczii and B. glauca. Bs have also been found by those from the Çug Pass, where all seven individuals other workers, Zakhariyeva & Makushenko (1969) of Johnson 277 collected at 2800 m were diploid, and Al-Mudarris (1973). The first reports are given whereas the single individual of Archibald 6530 from here of telocentric and acrocentric Bs in two individ- 3000 m was tetraploid. Although most species have uals of B. paradoxa; 85–606, 2n = 8 + 3 telocentric Bs only one ploidy level, Table 2 shows that there is some and 85–336, 2n = 16 + 2 acrocentric Bs. variation within a species. Since there is little or no morphological difference between diploids and tetrap- loids, the latter cannot be upheld (see above). DIFFERENT CHROMOSOME COUNTS Within Bellevalia, ploidy levels are known to vary. The different ploidy levels found in Bellevalia, Von Bothmer & Wendelbo (1981), who studied 45 pop- together with B chromosomes and other structural ulations from 15 provisionally named species from abnormalities, suggest that the genus is still evolving. eight different countries including Turkey, found both It is well known that geophytes are well-adapted to diploid and tetraploid counts for the Turkish endemic chromosome change and there are many examples of B. tauri. Their study also included 17 counts of Ira- different ploidy levels within a species, e.g. in Crocus, nian plants identified as B. glauca where five plants where even the basic number is sometimes variable had 2n = 8; one 2n = 8 + 1–2B; one 2n = 8 + 2–3B; four within a species (Brighton, Mathew & Rudall, 1983). 2n = 16; one 2n = 16, 17; two 2n = 24; one 2n = 24 + 1, Muscari, a genus closely related to Bellevalia, has 4–5B and one 2n = 32. This shows a complete poly- chromosome numbers based on x = 8. Dalgıç (1991), ploid range from diploid through to octoploid within who studied material from the three species found in a single species. More recently, investigations of European Turkey reported 2n = 16, 27, 36 and 54, B. brevipedicellata by Tzanodakis et al. (1991) whereas the Anatolian species investigated by reported 2n = 8 from western Crete and 2n = 16 from Johnson, Özhatay & Garbari (1996) was mostly dip- eastern Crete. loid, 2n = 16. Although the count of 2n = 24 for B. edirnensis by It is perhaps rather more unusual to find a genus Özhatay et al. (1991a, b) was the first hexaploid record such as Bellevalia which has such a range of ploidy for Turkish material, there were already 14 recorded levels which are all based on x = 4. hexaploid counts in several other species from Egypt, Dicentric chromosomes are uncommon in plants Afghanistan, Israel and Iran (Özhatay et al., 1991b). and due to the bridges that are often formed when To date, B. longistyla is the only octoploid species in they divide during mitosis, they are not usually stable. Turkey and is often aneuploid. This frequently occurs They have been found previously in genera such as

Narcissus by Darlington & Wylie (1952) and Agropy- incelenmesi. Turkish Journal of Biology 23: 357–368 (in ron by Hair (1952). More recently, Östergren & Öster- Turkish). gren (1982) and Jones & Colden (1997) reported them Darlington CD, Wylie AP. 1952. A dicentric cycle in Narcis- in Tradescantia. sus. Heredity Supplement 6: 197–213. Davis PH, Mill RR, Tan K. 1988. eds. Flora of Turkey and the East Aegean islands, Vol. 10. Edinburgh: Edinburgh Univer- SUMMARY AND CONCLUSION sity Press. 317–428. A range of ploidy levels occurs in Bellevalia, with Feinbrun N. 1938–39. A monographic study on the genus sometimes more than one level occurring within a spe- Bellevalia Lapeyr. Palestine Journal of Botany 1: 336– cies. The larger, more common tetraploid plants of 409. Garbari F. 1981. Il cariotypo-typus, nouvo concetto della B. paradoxa (2n = 16) have probably arisen from the Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 diploids (2n = 8) which are very similar phenotypi- citosistematica. Acta Biologica 58: 255–264 (in Italian with cally. Generally, the karyotype is remarkably stable, English abstract). with aneuploidy occurring only at the octoploid level. Govaerts R. 1996. World checklist of seed plants. Antwerp: B chromosomes were found in 13 individuals, two Belgium: Continental publishing. 2: 85–86. Güner A, Özhatay N, Ekim T, Bas¸ er KHC. 2000. eds. Flora occurrences of which in B. paradoxa were unusually of Turkey and the East Aegean islands Vol. 11. Edinburgh: either telocentric or acrocentric rather than metacen- Edinburgh University Press, 407–512. tric. The instances of B chromosomes, aneuploidy and Hair JB. 1952. The origin of new chromosomes in Agropyron. rare unstable structural changes do not play any sig- Heredity Supplement 6: 197–213. nificant role in the chromosomal evolution of the Johnson MAT. 1994. Cytology of three new geophytes from genus. Turkey. Kew Bulletin 49: 491–498. Johnson MAT, Brandham PE. 1997. New chromosome num- ACKNOWLEDGEMENTS bers in petaloid monocotyledons and in other miscellaneous angiosperms. Kew Bulletin 52: 121–138. I thank Brian Mathew (Kew) who originally suggested Johnson MAT, Güner A. 2002. Iris stenophylla Hausskn. & this study and provided some of the living material, Siehe ex Baker from Turkey and its cytology. Botanical Jour- Neriman and Engin Özhatay (Istanbul) and Jim and nal of the Linnean Society 140: 115–127. Jenny Archibald for plant material. Thanks are due to Johnson MAT, Özhatay N, Garbari F. 1996. The genus several college-based students for preparing some of Muscari (Hyacinthaceae) in Turkey: taxonomy, distribution the microscope slides, also to Adil Güner, Mehmet and chromosome analysis. In: Öztürk M, Seçmen Ö, Görk G, Koyuncu and Hayri Duman for taxonomic discussions eds. IVth Plant life in Southwest and Central Asia sympo- and to Peter Brandham for his helpful suggestions and sium. Ege University, Turkey. 1: 34–53. for photographing the two inflorescences of cultivated Jones K, Colden C. 1997. A dicentric cycle with a terminal B. paradoxa (Figure 1). centromere in Tradescantia. Nucleus 40: 101–114. Mirici S, Arslan O. 1994. Bellevalia cinsinin bazı endemik REFERENCES türlerinde karyolojik çalıs¸ malar. XII. Ulusal Biyoloji Kon- gresi (6–8, V11, 1994, Edirne) 11: 261–265. (in Turkish). Al-Mudarris HE. 1973. Cytological studies on the genus Bell- Östergren G, Östergren K. 1982. Transmissible dicentric evalia Lapeyr from Iraq. Bulletin of the College of Science, chromosomes in experimental material of Tradescantia and Baghdad 14: 177–186. some reflections on multicentric chromosomes and diffuse Bowen CC. 1956. Freezing by liquid carbon dioxide in making kinetochores. Hereditas 97: 328. slides permanent. Stain Technology 31: 87–90. Özhatay N, Johnson MAT. 1996. Some karyological remarks Brandham PE, Johnson MAT. 1977. Population cytology of on Turkish Allium sect. Allium, Bellevalia, Muscari and structural and numerical chromosome variants in the Ornithogalum subg. Ornithogalum. Bocconea 5: 239–249. Aloineae (Liliaceae). Plant Systematics and Evolution 128: Özhatay N, Johnson MAT, Mathew B. 1991a. Chromosome 105–122. numbers of Turkish Bellevalia L. species including a new Brighton CA, Mathew B, Rudall P. 1983. A detailed study hexaploid from European Turkey. Botanika Chronika 10: of Crocus speciousus and its ally C. pulchellus (Iridaceae). 813–818. Plant Systematics and Evolution 142: 187–206. Özhatay N, Johnson MAT, Mathew B, Dalgıç G. 1991b. A Dalgıç G. 1991. Cytotaxonomic studies on the genus Muscari. new hexaploid Bellevalia (Hyacinthaceae) from European European Turkey. Botanica Chronika 10: 819–825. Turkey. Botanical Journal of the Linnean Society 107: 89– Dalgıç G, Bas¸ ak N. 1996. Chromosome numbers of some pet- 99. aloid monocots from European Turkey. In: Öztürk M, Seç- Özhatay N, Sadıkogˇ lu N, Johnson MAT. 2002. Index to men Ö, Görk G, eds. IVth Plant Life in Southwest and Turkish plant chromosome numbers. In: Güner A, Özhatay Central Asia symposium. Ege University, Turkey. 1: 54–62. N, Ekim T, Bas¸ er KHC, eds. Flora of Turkey and the East Dane F. 1999. Hekzaploid (2n = 24) Bellevalia edirnensis N. Aegean islands. Vol 11. Edinburgh: Edinburgh University Özhatay & Mathew in pollen mitozu ve polen morfolojisinin Press, 407–512.

Persson K, Wendelbo P. 1979. Bellevalia hyacinthoides, a Wendelbo P. 1980. Notes on Hyacinthus and Bellevalia (Lil- new name for Strangweja spicata (Liliaceae). Botaniska iaceae) in Turkey and Iran. Notes from the Royal Botanic Notiser 132: 65–70. Gardens Edinburgh 38: 423–434. Tzanodakis D, Iatrou G, Kypriotakis Z, Christoudakis D. Wendelbo P. 1984. Bellevalia Lapeyr. In: Davis PH, ed. Flora 1991. Cytogeographical studies in some Aegean Liliaceae. of Turkey and the East Aegean islands, Vol. 8. Edinburgh: Botanika Chronika 10: 761–775. Edinburgh University Press, 64–74. Von Bothmer R, Bentzer B. 1973. Chromosome morphol- Wendelbo P. 1985. 16. Bellevalia Lapeyr. In: Townsend CC, ogy in Bellevalia dubia subsp. boissieri and B. trifoliata Guest E, eds. Flora of Iraq. Vol. 8. Baghdad: Ministry of Agri- (Liliaceae) from Greece. Annales Musei Goulandris 1: 11– culture. 113–127. 13. Zakhariyeva OI, Makushenko LM. 1969. Chromosome Von Bothmer R, Wendelbo P. 1981. Cytological and morpho- numbers of Monocotyledons belonging to the families Lili- Downloaded from https://academic.oup.com/botlinnean/article-abstract/143/1/87/2433618 by guest on 11 September 2019 logical variation in Bellevalia. Nordic Journal of Botany 1: aceae, Iridaceae, Amaryllidaceae and Araceae. Botanichestii 4–11. Zhurnal 54: 1213–1227.