Pleione 15(1): 61 - 68. 2021. ISSN: 0973-9467 © East Himalayan Society for Spermatophyte doi:10.26679/Pleione.15.1.2021.061-068 Recircumscription of noltiei Peruzzi, J.-M. Tison, A. Peterson & J. Peterson ()

Mrinmoy Midday, Jayanta Ghosh and Debabrata Maity1 Taxonomy and Biosystematics Laboratory, Department of Botany, University of Calcutta, 35 Ballygunge Circular Road, Kolkata - 700 019, West Bengal, India 1Author for correspondence: [email protected] [Received 17.03.2021; Revised 21.04.2021; Accepted 24.04.2021; Published 30.04.2021]

Abstract

The taxonomy of Gagea noltiei Peruzzi, J.-M. Tison, A. Peterson & J. Peterson (≡ Lloydia delicatula Noltie) (Liliaceae) is revisited and the species is recircumscribed. Gagea serotina (L.) Ker.- Gawl. var. parva (C.Marquand & Airy Shaw) D. Maity, M. Midday & J. Ghosh, comb. nov. et stat. nov. is proposed for Lloydia serotina f. parva C. Marquand & Airy Shaw. Key words: Gagea, Lloydia delicatula, Monophyly, Recircumscription, Taxonomy, Sikkim Himalaya

INTRODUCTION The geophytic alpine bulbous Gagea noltiei Peruzzi, J.-M. Tison, A. Peterson & J. Peterson ( ≡ Lloydia delicatula Noltie) of the Lily family (Liliaceae) was described by Noltie (1993) to accommodate some unique ‘dwarf elements’ of the genus usually growing on ‘mossy turf on boulders and exposed ridges; scree and rock ledges; occasionally meadows’ at elevation between 3600 – 4600 m amsl (Noltie 1993: 56). Since the time of Sir J. D. Hooker (1892) the genus Lloydia Salis. ex Rchb. suffers from many taxonomic discrepancies, evidently due to less concentration on this genus by the contemporary botanists, poor specimen preservation, mostly without reliable field data, coupled with scarce collections of this tiny bulbous herb. However, Hara (1966), Dasgupta & Deb (1986) and Dasgupta (2006) contributed appreciably to the taxonomy of this genus. In recent past Noltie (1993) studied extensively the diversity of the genus in the Eastern Himalaya and made noteworthy contribution through recognizing of new species as well as new synonym. He tried to resolve the taxonomic discrepancies of the Eastern Himalayan members through rigorous study of herbarium materials deposited at K, E, BM and CAL. He had elucidated several morphological traits like colour and posture of flowers, nectary and approach of midrib towards apex, etc., useful to diagnose the members under this genus. In his revision he had described Lloydia delicatula (now Gagea noltiei) and had distinguished it from L. serotina var. parva (C. Marquand & Airy Shaw) H. Hara (in Bull. Univ. Mus. Univ. Tokyo 2: 166. 1971) by a number of characters like flower posture, tepals length, shape, apex and midrib and most importantly the presence or absence and position of nectary. Noltie “first recognized the tiny ‘Lloydia’ as distinct in the herbarium and was then thrilled to see it for…[himself] growing at the edge of the East Ratong glacier in NW Sikkim in 1992" (pers. comm., in email to senior author, October 2020). Evidently, he has examined a considerable number of herbarium specimens along with his own collections. No doubt his field experience helped him immensely in recognizing the new species. He has also published illustration of G. noltiei (Noltie 1993: 54). Recently, we have observed many populations of Gagea on alpine slopes in North Sikkim. Fortunately, all populations were either in full bloom or in fruiting stages and thus 62 Recircumscription of Gagea noltiei taxonomic characterization was more reliable. After examination of specimens and comprehensive literature search (Hooker 1892; Hara 1966; Dasgupta & Deb 1986; Dasgupta 2006; Noltie 1993, 1994; Xinqi & Turland 2000) one group of specimens was identified as Gagea noltiei (Plate – I; Figure 1) whereas the other was recognized as L. serotina var. parva (Figure 2). Field observation provides opportunity to compare both the taxa more elaborately. During our field study we noticed a number of significant characters which could contribute significantly to the taxonomy of G. noltiei. More precisely, recircumscription of G. noltiei becomes essential with the presently observed important traits. This situation has motivated us to examine directly the type specimens of the species deposited at CAL including the specimen of W.W. Smith who recognized the uniqueness of his specimen (W.W. Smith 3468, acc. no.-CAL485114) and commented on herbarium as “Lloydia serotina Rchb. var. sikkimensis minima” but did not publish validly. In the protologue the tepals apices mentioned as narrow subacute and the same has been illustrated accordingly (Noltie 1993: 54; Plate - I: G,H,I), however, the tepals apices are definitely rounded (-obtuse). The midrib though riches apex, but in some tepals it is stopping short to apex. Importantly, one lateral vein on either side of the midrib is 2 rd running from tepal base to nearly /3 of total tepal length. The filaments in the presently collected specimens are significantly smaller, in contrast anthers are quite bigger in size. Fruits are considerably larger (3.5 – 4 × 2.4 – 3.4 mm) in the recently observes specimens. Furthermore, the seed are characterized for the first time in this species. Thus, a new illustration with most of the important plant parts has been provided (Figure 1). Besides, photo plates with images of live of G. noltiei are incorporated for convenient recognition. Subsequently, examination of type specimens of this species at CAL is also corroborating our observation (particularly tepal characters) and thus the species is recircumscribed with taxonomic judgment. It is a part of the nature of taxonomy that as more specimens become available the original description has to be widened to include additional variations (Noltie, pers. comm., in email to senior author, October 2020). The genus Gagea Salisb. with its around 100 species is distributed in subtropical, temperate and alpine regions of Europe and Asia (Levichev 1999; Mabberley 2017), though the number of species often varies between 70 to nearly 275 depending on the opinion of different authors (see Peterson et al. 2008; Peruzzi et al. 2008; Zarrei et al. 2009). In India the genus is exclusively Himalayan and counts only 13 species (Dasgupta & Deb 1986; Dasgupta 2006; Karthikeyan et al. 1989; Sinha et al. 2019). Sikkim shelters seven species of Gagea, mostly in the slopes of temperate and alpine forests (Srivastava 1996; Maity et al. 2018). Dasgupta (2006) did not consider G. noltiei as distinct species and treated as synonym of L. serotina. However, G. noltiei is a well-recognized species with important morphological features of its own (Table 1). In this article we accept G. noltiei as a good species and the revised description of G. noltiei is presented with amended characters for proper circumscription and correct identification. Moreover, detail illustration and field images are also incorporated for easy recognition. In addition, the comparison of most important morphological characters of G. noltiei with its close relative L. serotina var. parva is presented in Table 1. The preceding name is transferred to the genus Gagea to accomplish taxonomic outcome. MATERIALS AND METHODS The plant specimens were collected from interior valleys of the high Himalayan mountains of North Sikkim. Both the flowering and fruiting stages were collected through rigorous survey. Photographs were taken in the field for better understanding. Specimens were dried, fumi- gated and herbarium specimens were prepared following the standard method. The voucher specimens are deposited at CUH. All previously collected specimens deposited at CAL, BSHC and CUH were also examined. Detailed illustrations of both vegetative and floral parts were Mrinmoy Midday et al. 63 prepared using a stereomicroscope (Leica EZ4E). Recently collected materials were com- pared with type specimens deposited at CAL using the morphological features that have been used as diagnostic traits for the species. Relevant field data available on herbarium specimens were considered. All pertinent literature including protologues were critically examined for proper circumscription.

OBSERVATION Taxonomic treatment: Gagea noltiei Peruzzi, J.-M. Tison, A. Peterson & J. Peterson, Taxon 57(4):1212.2008. Lloydia delicatula Noltie, Edinburgh J. Bot. 50:55.1993 & Fl. Bhutan 3(1): 109. 1994. Type: Bhutan, Me La (S side), 14,500 ft, 09.6.1949, Ludlow, Sherriff & Hicks 20347 (holo, BM). [Paratypes: see Noltie, 1993: 56] [Plate – I; Figure 1] Perennial, bulbous herb in dense clumps; narrowly ovoid, to 5 mm diam; tunics papery, straw-colored; stem sheathed with papery remains of previous year-old leaf-bases at lower part; leaves 1 – 2, filiform, semi-terete, 7 – 20 × 0.4 – 0.7 mm, apex obtuse or rounded, dark, margin entire, shallowly channeled along adaxial side, gland-dotted, base sheathing with papery tunics; bracts 3, leafy, linear-lanceolate, 5 – 10 mm long, apex obtuse or rounded, margin entire, narrowly scarious, base sheathing; lower 2 bracts opposite or sub-opposite; lowermost to 1 cm long; flower solitary, erect, white, dark purple or pink tinged outside along midrib; tepals 6, in two whorls; outer 3 elliptic or rhombic, 4.4 – 5.6 × 1.4 – 1.7 mm, apex rounded (- obtuse), margin entire, base truncate, broad at middle, distinctly 3-veined; mid vein prominent, purple, reaching or ends before apex, 2 parallel veins arising from base, end much before apex, purple; inner 3 similar to outer, 4.4 – 4.6 × 1.4 – 1.6 mm; nectary distinct, thick, rounded, 0.7 – 0.85 mm above tepal base on mid vein, yellowish; stamens 6, opposite to tepals, in two whorls; outer: filaments slender, 1.5 – 2.9 × 0.25 – 0.3 mm, glabrous; anthers oblongoid, flattened, 0.4 – 0.75 × 0.35 – 0.4 mm, latrose, pink; inner: filaments 1.5 – 1.9 × c. 0.3 mm; anthers similar to outer; ovary ellipsoid or oblongoid-ovoid, trigonous, 1.5 – 2.4 × 1.1 – 1.5 mm, apex truncate, light green, suffused purplish at apex; style slender, 1 – 2.2 mm long, light green; stigma capitate, c. 0.25 mm, expanded; fruits ellipsoid-oblongoid, trigonous (-3-ribbed), 2.5 – 4.03 × 1.9 – 3.41 mm, edges slightly wavy, with persistent tepal bases; seeds curved- ovoid or reniform, 1.09 – 1.21 × 0.47 – 0.63 mm, light brown, reticulate. Distribution: INDIA: Sikkim; NEPAL, BHUTAN. Endemic to Eastern Himalaya. Habitat: Plants grow on open alpine pasture, grassland, mossy turf on rocks, open grassy hill slopes in between 3962 – 5029 m amsl. Flowering & Fruiting: June – August Specimens Examined: Gagea noltiei: INDIA: Sikkim, Lhonak La, 5029 m, 25.07.2018, Maity, Maiti, Ghosh & Midday 23782; Between Muguthang and Lake, 4400 m, Maity, Maiti, Ghosh & Midday 23792; Towards Muguthang, 4650 m, 05.8.2018, Ghosh 23795 [all at CUH]. Sikkim, Kapoor below Kinchinjunga, June 1887, King’s Coll. s.n.; Near Nathui La (Nathu La), 14000 ft (4267 m), 14.07.1910, W.W. Smith 3468 (note: Lloydia serotina Rchb. var. sikkimensis minima); Above Changu, 13000 ft (3962 m), W.W. Smith 3175 (note: Lloydia serotina Rchb. var. sikkimensis minima) [all at CAL]. 64 Recircumscription of Gagea noltiei

PLATE - I. Gagea noltiei: A. Habitat; B. Flowers (bird’s eye view); C. Flower (side view); D. Outer tepal (part), note position of nectary marked with yellow arrow; E. Outer tepal, note origin of lateral veins; F. Fruit; G. Seeds; H. Habit, note semiterete leaf with channel on adaxial side Mrinmoy Midday et al. 65 L. serotina var. parva INDIA: Sikkim, towards Gurudongmar, 4500 m, 01.9.2018, Midday & Ghosh 23863, 23865; Upper Thangu, 4350 m, 07.9.2018, Midday & Ghosh 23869 [all at CUH].

Figure 1. Gagea noltiei: A. Habit; B. Outer tepals; C. Inner tepals; D. Outer stamens; E. Inner stamens; F. Gynoecium; G. Fruit (from Maity, Maiti, Ghosh & Midday 23782-CUH) 66 Recircumscription of Gagea noltiei

Figure 2. Gagea serotina var. parva: A. Habit; B. Outer tepals; C. Inner tepals; D. Outer stamens; E. Inner stamens; F. Gynoecium (from Midday & Ghosh 23863-CUH).

DISCUSSION Gagea is largely a Eurasian genus with a few species in North Africa, comprising geophytic, perennial herbs. Until now, two dwarf forms of Gagea are available in this part of Himalaya, namely G. noltiei and G. serotina var. parva (see below), both are close relative though differ in number of characters (Table 1). G. noltiei is a distinct species and circumscribed here with distinct morphological traits. In recent past, the phylogeny of Gagea and Lloydia is resolved and Mrinmoy Midday et al. 67 these analyses support the monophyly of Gagea and Lloydia collectively (Peterson et al. 2007; Peruzzi et al. 2008; Zarrei et al. 2009). Importantly, these phylogenetic studies support the treatment Gagea serotina (L.) Ker.-Gawl. (a”Bulbocodium serotinum L.) instead of Lloydia serotina (L.) Rchb. and thus the new combination L. serotina f. parva C.Marquand & Airy Shaw (≡ L. serotina var. parva (C.Marquand & Airy Shaw) H. Hara) is desirable and is yet to be done. This combination is also essential to compare G. noltiei with its neighbor L. serotina var. parva. Thus, the following new combination is proposed. Gagea serotina (L.) Ker.-Gawl. var. parva (C.Marquand & Airy Shaw) D. Maity, M. Midday & J. Ghosh, comb. nov. et stat. nov. [Figure 2]

≡Lloydia serotina f. parva C. Marquand & Airy Shaw, J. Linn. Soc., Bot. 48: 228. 1929. ≡L. serotina var. parva (C. Marquand & Airy Shaw) H. Hara, Bull. Univ. Mus. Univ. Tokyo 2: 166.1971.

Table 1. Comparison of selected morphological characters between Gagea noltiei and G. serotina var. parva

Characters G. noltiei G. serotina var. parva Flower posture Erect Erect Bract 5 – 10 mm long 3.5 – 5.5 mm long Tepal appearance Thick, ± leathery Thin, papery length 3.6 – 5.7 mm 6.5 – 7.5mm shape Narrowly elliptic to narrowly Obovate, narrowly oblong or rhombic oblanceolate apex Rounded (-obtuse) Rounded midrib Reaching apex in few, in others Stopping short of apex stopping short of apex Nectary Conspicuous, c. ¼ way up tepals Basal or absent (0.7 – 0.85 mm above tepal base) Stamen filament 1.5 – 2.9 mm long 4 – 4.5 mm long anther ± circular, 0.4 – 0.5(0.8) mm, pink Oblongoid, 0.5 – 0.7 mm, yellowish Ovary 1.5 – 2.4 × 0.8-1.4 mm 2 – 2.28 × 0.8 – 0.9 mm Style 0.79 – 2.2 mm 1.5 – 1.72 mm Stigma Expanded, ± capitate Ovoid, deltoid Fruit shape Ellipsoid-oblongoid, trigonous Broadly oblongoid-ovoid, trigonous size 2.8 – 4.03 × 1.9-3.41 mm 3 – 4 × 2.5 – 2.8 mm

Acknowledgements Authors are thankful to the Ministry of Environment, Forest and Climate Change, Gov- ernment of India for financial assistance to our research program. The Department of Forests, Environment and Wildlife Management and Superintendent of Police, Gangtok are warmly thanked for permitting and supporting our field visit. We are grateful to the Director, Botanical Survey of India, Kolkata for giving the necessary permission to con- sult its herbarium (CAL). They are indebted to Dr. H. J. Noltie (E) for his kind help. The help and support received during field visit from Indian Army, ITBP, GREF-Thangu post are gratefully acknowledged. They also thank Mr. Umed Singh, Gangtok and Mr. Ringxing, Thangu for their help in organizing the field trips. Pritha Basu is warmly thanked for her help. 68 Recircumscription of Gagea noltiei LITERATURE CITED Dasgupta, S. 2006. Liliaceae. In: Singh, N.P. & Sanjappa, M. (eds.), Fascicles of Flora of India. Fascicles 23. Botanical Survey of India, Kolkata. pp. 60 – 87. Dasgupta, S. & Deb, D.B. 1986. Taxonomic revision of the genus Lloydia (Liliaceae) in India and adjoining region. J. For. 9(2): 104 – 112. Hara, H. (ed.) 1966. Flora of Eastern Himalaya. First Report. University of Tokyo Press, Tokyo. Hooker, J.D. 1892. Liliaceae. In: Hooker, J. D. (ed), The Flora of British India. Vol. 6. L. Reeve & Co., Kent, London. Pp. 299 – 362. Karthikeyan, S.; Jain, S.K.; Nayar, M.P. & Sanjappa, M. 1989. Florae Indicae Enumeratio Monocotyledonae. Botanical Survey of India, Kolkata. Pp. 96 – 97. Levichev, I.G. 1999. Zur Morphologie in der Gattung Gagea Salisb. (Liliaceae). I. Die unterirdischen Organe. Flora 194: 379 – 392. Mabberley, D. J. 2017. Mabberley’s Plant-Book, A portable dictionary of plants, their classification and uses, 4th edn. Cambridge University Press, Cambridge. P. 375. Maity, D.; Maiti, G.G. & Chauhan, A.S. 2018. Flora of Kanchenjunga Biosphere Reserve, Sikkim. Botanical Survey of India, Sikkim. Pp. 738 – 741. Noltie, H. J. 1993. Notes relating to the Flora of Bhutan: XX. Lloydia (Liliaceae). Edinburgh J. Bot. 50: 51 – 57. Noltie, H. J. 1994. Flora of Bhutan. Vol. 3(1). Royal Botanic Garden, Edinburgh. Pp. 108 – 111. Peruzzi, L.; Tison, J-M.; Peterson, A. & Peterson, J. 2008. On the Phylogenetic Position and Taxonomic Value of Gagea trinervia (Viv.) Greuter and Gagea sect. Anthericoides A. Terracc. (Liliaceae). Taxon 57(4): 1201 – 1214. Peterson, A.; Levichev, I.G. & Peterson, J. 2008. Systematics of Gagea and Lloydia (Liliaceae) and infrageneric classification of Gagea based on molecular and morphological data. Mol. Phylogen. Evol. 46: 446 – 465. Sinha, B.K.; Dash, S.S. & Singh, P. 2019.Plants of Indian Himalayan Region (An Annonated Checklist & Pictorial Guide). Botanical Survey of India, Kolkata. Pp. 709 – 712. Srivastva, R.C. 1996. Liliaceae. In: Hajra, P.K. & Verma, D.M. (eds.), Flora of Sikkim, Vol 1 (). Botanical Survey of India, Calcutta. Pp. 142 – 163. Xinqi, C. & Turland, N. J. 2000. Lloydia. In: Wu, Z.Y. & Raven, P.H. (eds.), Flora of China. Vol. 24 (Flagellariaceae through Marantaceae). Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. Pp. 121 – 123. Zarrei, M.; Wilkin, P.; Fay, M. F.; Ingrouille, M. J.; Zarre, S. & Chase, M.W. 2009. Molecular systematics of Gagea and Lloydia (Liliaceae; ): implications of analyses of nuclear ribosomal and plastid DNA sequences for infrageneric classification. Ann. Bot. 104: 125 – 142.