Fritillaria phitosia Kamari, Zahos & Siagou, 2017

Kamari, Georgia, Zahos, Athanasios & Siagou, Ioanna, 2017, A new yellow-flowered Fritillaria species (Liliaceae) from Mt. Tisseon, continental Greece and its taxonomic relationships, Phytotaxa 328 (3), pp. 227-242 : 231-236

Fritillaria phitosia Kamari, Zahos & Siagou sp. nov. ( Figs. 3A–E , 6C–D )

Fritillaria phitosia has some morphological relations with F. euboeica and the other yellow to yellowish-green flowered Fritillaria species occurring in Greece, but it is easily distinguished by its flowers and tepals shape, which is mainly defined by the position of the nectaries (ca. 3–4 mm distance from the base of the tepals), and by its divided style (up to 1/2). The new species is also distinguished mainly by its tepals’ colour from the related species, F. sporadum , F. obliqua Ker Gawler (1805: 857) and F. ehrhartii , which have dark purplish flowers, at least externally. Additional differences between the new species and a) the above taxa are presented in Table 1 and b) the yellow to yellowish-green flowered taxa in the taxonomical key.

Type: — GREECE ( EC). Nomos Magnissias, Mons Tisseon, in declivibus montis supra viam, 18 km a pago Milina versus vicum Trikeri ; in Quercetis cocciferosis (pseudomacchia), solo calc., 30–100 m a.s.l., 39 o 05΄56.53΄΄ N, 23 o 06΄15.37΄΄ E, 9 March 2013, Dimitrios Phitos, Georgia Kamari, Athanassios Zahos & Ioanna Siagou No 27712 (holotype herb.- Phitos & Kamari, UPA!, isotypes ACA!, PAL-GR!) .

Perennial, bulb up to 2 cm in diameter. Stem up to (12–)15–28(–33) cm high. Leaves (3–)4–7(–8), glaucous, lanceolate to oblanceolate, the lower (4–)6–10(–14) × 1.9–2.5(–3) cm, usually alternate; the uppermost 2–5 × 0.2–0.4 cm, lanceolate to linear lanceolate. Flowers usually solitary, rarely two, broadly and shortly campanulate, often wide opening at the mouth, bright yellow, rarely with green nerves or purple spots at the outer base of the tepals. Outer tepals (1.7–)2–2.5(–3) × 0.8–1.0 cm, narrowly elliptic to rhomboid, acute to obtuse; the inner usually broader up to 1.0(–1.2) cm than the outer, obtuse, with small papillae at the apex. Nectaries lanceolate, 4–5 × 1–2 mm, green to dark green, 3–4 mm distante from the base of the tepals. Style 0.8–0.9 cm long, 3-fid to 1/3–1/2, glabrous, or rarely sparsely papillose. Capsule subglobose to globose, unwinged.

Karyology:—The cytology of the genus Fritillaria has been studied for many years due to the interest on its large chromosomes and its vast genome size ( Darlington 1935, 1937, Frankel 1940, La Cour 1978). Indeed, Fritillaria 1 C values (DNA content of the unreplicated haploid chromosome complement) are among the largest reported for all angiosperms ( Bennett & Smith 1976, Zaharof 1989, Sharma & Raina 2005, Peruzzi et al. 2009, Samaropoulou et al. 2016). The karyotype is quite stable, asymmetrical (most chromosomes are acrocentric to subtelocentric) and usually diploid, with a basic chromosome number of x = 12. Only a few species deviate from this, with x = 9 (3 species), x = 11 (2 species) and x = 13 (2 species), but without a special pattern ( Darlington 1937, Noda 1964, Li & Shang 1989, Jafari et al. 2014). Individuals of Fritillaria phitosia from the type locality show a chromosome number of 2n = 24 ( Figs 4A & 4B ). Thus, the species is diploid with long (11.5–22.5 μm) chromosomes and its chromosome complement consists of two longer pairs, the longest being metacentric (m) and the second submetacentric (sm), while the remaining ten pairs are acrocentric (st) to subtelocentric (t) chromosomes, one of which has satellited short arms. Therefore, its karyotype formula consists of: 2m + 2sm + 6st + 12t + 2 SAT-t = 24 chromosomes ( Fig. 4A ). Breaks often occur on the short arms of these marker t-chromosomes including the secondary constriction, and looks like B-chromosome ( Figs 4A–B ). Such a marker-chromosome pair does not occur in all the other yellow-flowered Fritillaria species examined, but has, however, been observed in some Ftitillaria taxa with more or less purple flowers, among other in F. ehrhartii ( Runemark 1970, Bentzer et al. 1971, Kamari 1984a), F. obliqua s.l. ( Kamari 1984a), F. sporadum ( Kamari 1984b) .

Phenology:—Flowers occurring from the beginning to the end of March, and capsules from May to June.

Etymology:—The species is named after Dimitrios Phitos, Professor Emeritus of Plant Systematic and Phytogeography at the University of Patras, who has been working on the Greek Flora for more than sixty years and is the mentor who encouraged us and supported our work with the attractive genus Fritillaria .

Distribution:— Fritillaria phitosia is currently known only from the type population (two localities) on Mt. Tisseon, on Magnissia peninsula (East-Central, Greece). It is distributed along the road from the villages Milina to Trikeri ( Fig. 5A ). A more thorough investigation around the Magnissia peninsula and on both sides of Mt. Tisseon showed that F. phitosia is a local endemic restricted only to the south-western slopes of the mountain. Most yellow-flowered Fritillaria taxa, occurring in Greece have a restricted distribution on an island or even on a mountain, except for F. euboeica and F. conica , both of which grow in continental Greece and thus have a wider distribution ( Fig. 2 ). In particular, F. conica , which grows in SW Greece, Peloponissos, was initially known only from Messinia peninsula, from Pilos to Methoni and southwards up to the small island Sapientza ( Kamari 1996). Later, it was referred from Malea Peninsula ( Tan et al. 2006, Greekflora.gr 2005 onwards). We have also discovered it on Mt. Kalathion ( Fig. 1D ) in the NW part of Mt. Taigetos ( Kamari & Phitos 2009).

Habitat and Ecology:—The new species colonizes only the north-western facing slopes of Mt. Tisseon and grows on limestone substrate, between 30 to 150 m a.s.l., among or under Pistacia lentiscus Linnaeus (1753: 1026) and Quercus coccifera Linnaeus (1753: 995) shrubs ( Fig. 5B ), where some other bulbous plants also coexist, such as: Arisarum vulgare Targioni Tozzetti (1810: 67) , Cyclamen graecum Link (1835: 573) , Gagea peduncularis ( Presl & Presl 1822: 150) Pascher 1904: 114 , Muscari commutatum Gussone (1827: 425) , Narcissus tazetta Linnaeus (1753: 290) , Neotinea lactea ( Poiret 1798: 594) Bateman et al. 1997: 122 ), Ophrys bilunulata Risso (1844: 463) subsp. punctulata ( Renz 1928: 265) Paulus (2014: 272) , Ophrys oestrifera Marschall von Bieberstein (1808: 369) , Romulea linaresii Parlatore (1839: 38) s.l., etc.

Suggested conservational status:—The occupation area of Fritillaria phitosia is about a 50 ha area, and its population appears to be divided in two subpopulations, each of which is estimated to be comprised of ca. 500 and 1000 mature individuals with a few, sparsely growing plants between them. In total, the population size was estimated to be less than 1800 mature (flowering) individuals, varying per year according to climate fluctuations, not showing, however, a decreasing trend over the years. No serious anthropogenic or grazing effects were observed on the size and quality of the population during the seven years of monitoring. Only in 2015 we observed many plants (more than 30%) to have been attached by the scarlet or red lily beetle ( Lilioceris lilii Scopoli, 1763 ), which destroyed the whole plant (leaves, stem and flower), while domestic herbivores, especially goats, grazed only upon the flowers. It must be noted that this loss per year was estimated to be at least 25% of the reproductive units of the population. Following the IUCN (2016) criteria, the taxon should be categorized as Endangered (EN), on the basis of its restricted distribution, estimated to be less than 5000 km 2 [B1a,c(i-iv) + B2a,c(i-iv)] and the fact that no more than 1800 mature individuals were counted, during seven years of monitoring. It should be noted that the Fritillaria species are long-lived perennial bulbous plants and each mature individual (i.e. 3–4 years old) does not produces flower(s) every year, therefore population degradation, due to reduced sexual reproduction are not easy to estimate. Concerning the conservation status of the Greek Fritillaria taxa, so far, only 5 are included in the European Union Directive 92/43 for the Nature and 13 taxa in the Red Data Books of the threatened plants of the Greek flora ( Phitos et al. 1995, 2009), 4 of which are categorized as Endangered (EN), 7 as Vulnerable (VU), 1 as Near Threatened (NT) and 1 as Rare (R). None of them is listed in the CITES (2013) catalogue for Greece.

Further specimens seen (paratypes):— GREECE ( EC). Nomos Magnissias: Mons Tisseon, in declivibus montis supra viam, 20 km a pago Milina versus vicum Trikeri ; in Quercetis cocciferosis (pseudomacchia), solo calc., 50–150 m a.s.l., 39 o 05΄44.31΄΄ N, 23 o 05΄34.05΄΄ E, 9 March 2013, D. Phitos, G. Kamari, A. Zahos & I. Siagou No 27713 (Herb. - Phitos & Kamari, UPA!) ; ibidem, 15 March 2016, S. Samaropoulou, I. Patrikios, A. Zahos & I. Siagou No 8192 sub Samaropoulou SF1101 ( ACA!) .

Taxonomic relationships:—Except for Fritillaria phitosia , all other Fritillaria species occurring in Greece with yellow or yellowish-green tepals (perianth segments) have conical to narrowly campanulate and not tessellated flowers. All the species growing on East Aegean Islands have undivided styles, and all of the west Aegean and continental Greece species possess more or less 3-fid styles. The two yellow-flowered Fritillaria species, endemic to continental Greece, F. euboeica ( Fig. 1C ) and F. conica ( Fig. 1D ), have no more than by 1/3 divited, slender styles. Taller plants of F. euboeica from C & N Evvia were described by Zaharof (1986: 727) as a separate species (‘ F. rixii ’), and they constitute in fact an ecotype of the typical species ( Kamari 1991a, 1991b). The most distinguished species among the yellow to yellowish-green flowered taxa, is F. bithynica ( Fig. 1E ), for subglobose capsules showing six wings ( Fig. 1I ). It is very similar to F. ehrhartii var. prassinantha Kamari (1991a: 259) from Kiklades islands (Tinos, Andros), where among the typical plants of the taxon, several individuals’ flowers are of a yellow to yellowish-green or intermediate colour ( Fig. 6B ), but always showing unwinged capsules ( Kamari 1991a). Fritillaria bithynica shows a wide distribution from Bithynian Olimbos of Turkey southwards to SW Anatolia ( Rix 1979, 1984) up to the East Aegean islands Samos and Ikaria. Rix (1979, 1984) reported that F. bithynica , showing unwinged capsules, also occurs on Chios island. Unlike Rix (1979, 1984), we consider that the wings of the capsules are a very significant, stable morphological feature, and the specimens referred by Rix (1979, 1984) as F. bithynica from Chios isl. showing unwinged capsules, certainly belong to F. pelinaea ( Fig. 1G & 1H ), which was originally collected by Kamari & Christodoulakis on Mt. Pelineon, above Spartounda, in February of 1979 as bulbs, and was rediscovered by us in April of 1990 in full flowering. It is easily distinguished from F. bithynica and all other yellow-flowered Fritillaria species by its robust stem and broadly ovate-lanceolate, somewhat fleshy, green, amplexicaule leaves, as well as by its broadly cylindrical, unwinged capsule ( Fig. 1J ) ( Kamari 1996, Kamari 2009a). In addition, the basal and cauline leaves are usually opposite or sometimes in a whorl of three ( Figs 1G & 1H ). Dimopoulos et al. (2013) considered F. pelinaea as a synonym of F.carica only with the comment ‘as proven under cultivation’. It is known, however, that F. carica also grows on Chios island and probably the cultivated material which was seen by A. Strid actually belonged to that taxon

Recently (on March 28, 2016), we checked with our colleague P. Saliaris F. pelinaea on Mt. Pelineon ( Fig. 1G , Appendix 1) and also the new subpopulation previously discovered at lower altitudes on the NW part of Mt. Pelineon (Appendix 1). The plants were somewhat smaller, but showing stable morphological characters ( Fig. 1H ). We also measured and monitored the population of F. carica on Mt. Provatas, Chios ( Fig. 1B ).

Related to F. phitosia are also some taxa with dark-purple flowers, at least on the outside: F. sporadum ( Fig. 6A ), F. ehrhartii ( Fig. 6B ) and F. obliqua Ker Gawl. s.l. ( Fig. 6E ), all Greek endemics in the C & W Aegean area. Their main morphological similarities and differences are given in Table 1. It is interesting that on some individuals of F. phitosia we observed purple spots on the outer base of the tepals ( Fig. 3D ), or rarely, mostly in maturity, the tepals had reddish to purple veins ( Fig. 6C ) or became orange ( Fig. 6D ). We estimated that 4–5% of the plants have purple spots and this percentage appears to be this stable during seven years of monitoring. We have also often observed this phenomenon in F. euboeica ( Kamari & Kalogeropoulos 2009) and in F. forbesii from Samos island ( Kamari 1996), and this was also noticed by Rix (1975, 1979) on material from SW Anatolia. Additionally, in March 2013 we found one individual to have purely purple flower only on the outside, but, since then we have not found any similar plants, despite our best efforts. Such purple spots or even stripes on the flowers are also referred by Rix (1979) on about two thirds of the individuals from some populations of F. bithynica from W Anatolia. Respectively, the populations of some Fritillaria species, typically characterized by completely dark, or at least externally purplish flowers, include, sporadically, yellow or yellowish-green individuals. Kamari (1991a) noticed this phenomenon in populations of F. ehrhartii from the islands Tinos and Andros, which was found to include some plants with yellowish-green flowers, which has been described as a separate variety, F. ehrhartii var. prasinantha , since all the intermediate colors were observed in the same population ( Fig. 6B ). Later, the same phenomenon was observed among plants of F. obliqua subsp. obliqua from Kinosoura peninsula, Attiki (Kamari et al. 2009), in Evvia by E. Kalogiannis ( Fig. 6E ) and also in F. rhodocanakis ( Kamari 2009b) . Recently, it was also observed by G. Kofinas, in the population of F. epirotica Turrill ex Rix (1975: 160) from Mt. Smolikas ( Fig. 6F ), which is endemic to NW continental Greece (N Pindos range), as well as in many other taxa. The discovery of the new Fritillaria phitosia from continental Greece increase the taxa occurring in the whole territory to 31 (26 species and 5 subspecies), 9 of which are purely yellow-flowered and 5 of them are Greek endemics. The three yellow-flowered Fritillaria species of continental Greece have more or less 3- fid styles, while all the others from the East Aegean Islands have undivided styles. Additionaly, Fritillaria phitosia is the only yellow-flowered species with broadly campanulate flowers, like most purple-flowered species, while all the others have more or less conical campanulate ones.

It is remarkable that Greece constitutes the western distribution frontier of Fritillaria taxa with purely yellow or yellowish flowers in the Old Word.

Figures

FIGURE 1. Individuals of the yellow flowered Fritillaria species occurring in Greece. (A) F. sibthorpiana from Simi isl. (photo by Z. Antonopoulos); (B) F.carica from Chios isl., Mt. Provatas (photo by P. Saliaris & G. Kamari); (C) F. euboeica from Evvia isl., Mt. Dirphis (photo by I. Kofinas); (D) F. conica from Mt.Taigetos, above the village Elaeochorion (photo by G. Kamari); (E) F. bithynica from Samos isl., Mt. Kerkis (photo from cult. material by G. Kamari); (F) F. forbesii from Samos isl., Mt. Ampelos (photo from cult. material by G. Kamari); (G) & (H) F. pelinaea from Chios isl., Mt. Pelineon and Giannakis area respectively (photos by P. Saliaris & G. Kamari); (K) F. rhodia from Rodos isl., close to Tsabika’s monastery (photo by S. Samaropoulou). Capsules of: (I) F. bithynica from Samos isl. and (J) F. pelinaea from Chios isl. (photos from cult. material by G. Kamari).

FIGURE 2. Complete distribution map of all known yellow-flowered Fritillaria species occurring in Greece.

FIGURE 3. Fritillaria phitosia sp. nov. (A) flowering individual; (B) flowering individuals in their natural habitat; (C) inner face of a flower with anthers and 3-fid style; (D) outer face of a flower with purple spots at the base of the tepals; (E) inner face and shape of the outer and inner tepals with lanceolate nectaries; (F) capsules of mature individuals (photos by I. Siagou).

FIGURE 4. Microphotographs of mitotic metaphase plates of Fritillaria phitosia, 2n = 2x = 24. -Arrows indicate SAT-chromosomes and the fragments (like B-chromosomes) of the marker st-chromosomes. Scale bars = 10 μm.

FIGURE 5. (A) distribution map of Fritillaria phitosia sp. nov. on Mt. Tisseon of Magnissia peninsula; (B) Mt. Tisseon the natural habitat of F. phitosia.

FIGURE 6. (A) individuals of: Fritillaria sporadum in their natural habitat on Gioura isl., N Sporades (photo by G. Kamari); (B) F. ehrhartii fromTinos isl., Kiklades, typical and var.prasinantha from the same population (photo by G. Kamari); (C) F. phitosia with purple spots on the external base of the tepals and (D) having turned orange in maturity (photos by I. Siagou); (E) F. obliqua, a yellow-flowered form with purplish spots at the base of the tepals and a typical one (in background) from Mt. Kallimani, Oktonia area, Evvia isl. (photo by E. Kalogiannis); (F) typical and yellow-flowered form of F. epirotica from Mt. Smolikas, N Pindos range (photo by I. Kofinas).