HARVARD PAPERS IN BOTANY 3(1): 73-78. 1998.

NOTES ON CHINESE CARDAMINE (BRASSICACEAE)

Ihsan A. Al-Shehbaz and Yang Guang

Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299, U.S.A.

Abstract. Cardamine cheotaiyienii, a new species from Yunnan Province, is described and illustrated. The genus Loxostemon is reduced to synonymy of Cardamine. A new combination and two new synonyms are proposed.

Cardamine Linnaeus is a cosmopolitan genus of about 200 species distributed on all continents except Antarctica (Al-Shehbaz, 1988). It is represented in China by about 50 species, of which nearly 30 are endemic. As discussed below, the generic limits are expanded herein to include Loxostemon J. D. Hooker & Thomson. The present paper deals with some nomenclatural adjustments needed for the forthcoming treatment of the Brassicaceae for the Flora of China.

Cardamine cheotaiyienii Al-Shehbaz & G. Yang, nom. nov. et stat. Nov.

Synonym: Hilliella alatipes (Handel-Mazzetti) Y. H. Zhang & H. W. Li var. macranthus Y. H. Zhang, Acta Bot. Yunnan. 8: 403. 1986. TYPE: China, Yunnan. Malipo, Guan-gaw, 1000 m, 14 February 1940, C. W. Wang 86836 (holotype: KUN; isotype: IBSC). (Fig. 1.)

Herba perennis scaposa. Rhizoma crassa, cicatricibus petiolorum prominensitus. Folia basalia 2, trifoliolata; petiolis 5--30 cm longis, glabris; foliolis ovatis, 7--18 x 4--5 cm, supra glabris, infra sparse brevihirsutis, repandis vel repando-crenatis, minute ciliatis, nervis lateralibus mucronatis; petiolulis folioliorum terminalium 0.6--1.5 cm longis. Folia caulina nulla. Scapa 15--30 cm longa, racemis corymbosis, paucifloris, ebracteatis. Pedicelli floriferi tenues, 2--3.2 cm longi. Sepala oblonga, 5--6 x 2.5--3.5 cm, subsaccata. Petala alba, oblonga, 1.5--1.7 x 0.5--0.8 cm, apice rotundata; unguibus 1--2 mm longis. Fructus ignotis.

Herbs perennial, scapose. Rhizomes ca. 5 x 0.5 cm long, thick, with prominent petiolar scars. Basal leaves 2, trifoliolate; petiole 5--30 cm long, glabrous; leaflets ovate, 7--18 x 4--5 cm, adaxially glabrous, abaxially sparsely hirsute with thick hairs 0.5--0.8 mm long, base of terminal leaflet cuneate, that of lateral leaflets oblique, margin repand to repand-crenate, sparsely ciliate with hairs 0.1--0.2 mm long, apex obtuse to acute; lateral veins ending with mucros 0.3--0.5 mm; petiolule of terminal leaflet 0.6--1.5 cm long, that of lateral leaflets 2--6 mm; stem leaves absent. Scapes 15--30 cm long, glabrous, leafless; inflorescence a few-flowered, ebracteate corymbose raceme. Flowering pedicel slender, 2.0--3.5 cm long, glabrous. Sepals ascending, oblong, 5--6 x 2.5--3.5 mm long, erect, slightly saccate at base, glabrous. Petals white, oblong, 1.5--1.7 x 0.5--0.8 cm, erect, apex rounded; claw 1--2 mm. Filaments white, 5--7 mm long, erect; anthers oblong, ca. 2 mm. Ovary narrowly linear, glabrous; stigma capitate, entire. Fruit unknown.

Cardamine cheotaiyienii is named after Professor Cheo Tai-yien, an outstanding scholar of Chinese Brassicaceae. This species can be readily distinguished from all other Asian members of Cardamine by its few basal and no stem leaves, large flowers to 1.7 cm long, and flowering pedicels 2.0--3.5 cm long. The type collection has no fruits, and it is usually difficult to assign genera to flowering material of the Brassicaceae. Because trifoliolate leaves are found in only two genera of the family---Cardamine and Yinshania Y. C. Ma & Y. Z. Zhao (including Hilliella [O. E. Schulz] Y. H. Zhang & H. W. Li)---it was rather easy to determine the generic disposition of the new species. Cardamine cheotaiyienii was originally described as Hilliella alatipes var. macranthus by Zhang (1986), but its erect sepals, petals, and stamens; narrowly linear ovaries; broad placental area (becoming the winged fruit replum); and ciliate leaves are characteristic of numerous Cardamine species, and this character combination is not found in any member of the expanded Yinshania (see Al-Shehbaz et al., 1998). The brief Latin diagnosis given by Zhang (1986), as var. macranthus, is emended above. As shown below, H. alatipes is a synonym of C. fragariifolia O. E. Schulz, a very distinct species with several-leaved stems, much smaller flowers, to (6--)7--9(--10) mm long, and much shorter flowering pedicels, 5--9(--13) mm long. Furthermore, the genus Hilliella does not merit recognition, and as pointed out by Al-Shehbaz et al. (1998), it is indistinguishable from the earlier-published Yinshania. Yinshania has spreading sepals, petals, and stamens; globose to oblong ovaries; narrow placental area; and nonciliate leaves.

The type collection bears tags indicating that the collectors are Wang, Chang, and Liu, though the sheet label carries C. W. Wang (Wang Chi-wu) as the sole collector.

Cardamine fragariifolia O. E. Schulz, Bot. Jahrb. Syst. 32: 446. 1903. TYPE: CHINA. Hubei, 1885--1888, A. Henry 5803 (holotype: B, non vidi; isotypes: GH, K, non vidi).

Cardamine scoriarum W. W. Smith, Notes Roy. Bot. Gard. Edinburgh 11: 203. 1919. Cochlearia scoriarum (W. W. Smith) Handel-Mazzetti, Symb. Sin. 7: 359. 1931. TYPE: CHINA. Yunnan: flank of volcanic mountain to NW of Ten-yueh, 25 N, 7000 ft, June 1912, G. Forrest 8201 (holotype, E; isotype, K).

Cardamine smithiana Biswas, J. Bot. 76: 22. 1938. TYPE: China. Tibet (Xizang): Cong La, 2900 m, 25 July 1933, F. Ludlow & G. Sherriff 324 (holotype, BM).

Cochlearia alatipes Handel-Mazzetti, Symb. Sin. 7: 370. 1931. Syn. nov. TYPE: China. South West Hunan. In monte Yün-schan prope urbem Wukang, 1000 m, 12 June 1918, Handel-Mazzetti 12097 (holotype: WU; isotypes: E, W, WU).

Herbs perennial. Rhizomes 2--5 cm long, 3--8 mm wide, compact. Stems erect, (35--)50--100(--130) cm tall, 3--6 mm in diameter, often simple at base, branched or simple above, stout to rarely slender, glabrous or rarely puberulent; internodes (3--)5--10(--20) cm apart. Basal leaves lacking at flowering. Stem leaves (5--)7--10(--15), petiolate, trifoliolate, rarely lowermost ones with 4 or 5 leaflets, often simple at inflorescence; petiole 1--6(--10) cm long, wing 0.5--1.0(--1.5) wide, lowermost leaves on luxuriant specimens very rarely with auricles ca. 1 mm; petiolules 1--6(--11) mm long; leaflets subequal or terminal slightly or rarely considerably larger, ovate to lanceolate, rarely elliptic to subrhomboid or suboricular, (1.5--)3.0--8.0(--12.0) cm long, (1--)2--3(--5) cm wide, glabrous to sparsely or rarely moderately with appressed, antrorse simple trichomes 0.1--0.7 mm long, always ciliate at margin with trichomes 0.1--0.2 mm long, base cuneate to obtuse, that of lateral leaflets often oblique, margin coarsely to minutely serrate to crenate, rarely shallowly lobed or subentire with obscure teeth, the teeth distinctly mucronate, apex acute to acuminate or rarely acuminate-caudate. Racemes (5--)12- to 40(--60)-flowered, ebracteate; pedicels slender, straight, divaricate, 5--9(--13) mm long, glabrous or sparsely puberulent. Sepals oblong, 2.5--3.5(--4.0) mm long, 1.5--2.0 mm wide, erect to ascending, not saccate, glabrous. Petals purple to lavender or pink, rarely white, obovate or rarely obovate-oblong, (6--)7--9(--10) mm long, (2.5--)3.0--4.0 mm wide, rounded at apex, attenuate at base to a claw 1.5--2.0(--3.0) mm long. Filaments erect, 3--4(--5) mm long, tetradynamous; anthers (0.6--)0.7--1.0 mm long. Lateral nectar glands semilunar to ringlike. Pistil glabrous; style slender, ca. 1 mm; stigma entire. Fruits not seen.

Additional specimens examined: BHUTAN. Above Mongar, Grierson & Long 1998 (E); near Chendebi, Ludlow, Sherriff, & Hicks 17056 (BM, E); Pimi Pumthang, Cooper, Bulley, & Cheshire 4171 (BM); Lao, Trashi Yangsi Chu, Ludlow, Sherriff, & Hicks 20829 (BM); Chorten Cora, Lyon 9073 (E). CHINA. Hubei: without locality, H. J. Li 5879 (IBSC). Hunan: Long-shan Co., L. H. Liu 1554 (NAS). Guangxi: Bing Long, Miu Shan, N Luchen, R. C. Ching 6044 (IBSC, PE, W). Guizhou: Jiang-Kou Co., Z. S. Zhang et al. 401919 (PE); Yin-jiang Co., Z. S. Zhang et al. 401773 (PE); Lei-shan Co., Z. B. Jian et al. 50288 (KUN, PE). Sichuan: near the Sichuan-Hubei border, H. F. Zhou 108309 (IBSC); Omei Shan, F. T. Wang 23345 (GH), H. G. Xu 1222, 1223, 5568 (MO), D. H. Du 141 (NAS), T. Y. Zhou & G. J. Xu 446 (PE), H. C. Zhou 7844 (KUN), S. L. Sun 2486 (IBSC); Omei Shan, Lei-tung-ping, S. C. Sun & K. Chang 1022 (A); Omei Shan, Chi-li-po, S. C. Sun & K. Chang 938 (A); Omei Shan, Hungchunping, H. C. Chow 7844 ( A); Nan-chuan Co., J. H. Xiong & X. L. Zhou 91452 (IBSC). Yunnan: Yangbi Xian, W side of Diangcang Shan, Malutang in the vicinity of Chang Shan, 25 46' N, 100 01' E, Bartholomew et al. 452 (A, CAS, KUN, PE, US); between Shweli and Tengyueh valleys, 25 N, Forrest 7947 (E, K); Shweli-Salwei divide, 25 55' N, 99 45' E, Forrest 27035 (E, K); without locality, Forrest 18154 (K); Youn-shan Hsien, N. T. Tsai 51040 (A, IBSC, NAS).

Except for Cheo (1987), no other reference on Himalayan botany mentions C. fragariifolia. As shown above, the name has priority over the most commonly used C. scoriarum, and it is not clear why C. fragariifolia has been overlooked. The species occurs in India (Hajra and Chowdhery, 1993), but we have not examined any material from that country. The only material we examined from the Xizang provinces is the holotype of C. smithiana. However, the species (as C. scoriarum) has also been listed by Hajra et al. (1996) from Xizang (as Arunachal Pradesh, India). Because of the confused identity of the species, a detailed description and distribution is provided above. The species grows at 1000--3000 m, primarily in wet areas of forests and rocky places.

Cheo (1987) correctly treated C. fragariifolia and C. scoriarum as conspecific, but his treatment of these two and C. paucifolia Handel-Mazzetti as synonyms of C. trifoliolata J. D. Hooker & Thomson (Bhutan, India, Nepal, Sikkim), as well as the maintenance of C. smithiana as a distinct species, is incorrect. Cardamine trifoliolata is an entirely different species, readily distinguished from C. fragariifolia by its being a slender plant 5--20(--30) cm tall, and with white flowers, few stems leaves, and repand or obtusely lobed terminal leaflet 5--10(--15) mm long. As defined here, C. fragariifolia is a robust plant (35--)50--100(--130) cm tall, with purple to lavender or pink (rarely white) flowers, (5--)7--10(--15) stem leaves, and serrate to crenate terminal leaflet (1.5--)3.0--8.0(--12.0) cm long. Furthermore, C. paucifolia is readily separated from C. fragariifolia by its being a slender annual with 2 or 3 stem leaves, few-flowered racemes, white petals, and unwinged petioles. In contrast, C. fragariifolia is a robust perennial with (5--)7--10(--15) stem leaves, many-flowered racemes, purple to lavender or pink (rarely white) flowers, and winged petioles.

Handel-Mazzetti (1931) confused the flowering material of C. fragariifolia with plants of Cochlearia Linnaeus sect. Hilliella O. E. Schulz, as evidenced by his description of Handel-Mazzetti 12097 as Cochlearia alatipes. The type collection of C. alatipes has no fruits but has narrowly linear young ovaries; erect sepals, petals, and stamens; broad placental area; and minutely ciliate leaflets. All of these features are characteristic of numerous species of Cardamine, and no species of Cochlearia s.l. has this combination of characters.

Although Smith (1919) cited two syntypes (Forrest 8201 and Forrest 7947) in his original description of C. scoriarum, only Forrest 8201 carries Smith's hand-written annotation and designation as the type. Therefore, this latter collection is taken as the holotype. The original publication of Cochlearia alatipes cited Handel-Mazzetti 1209, instead of Handel-Mazzetti 12097, as the type. One of the two type sheets at WU has Handel-Mazzetti's hand writing as "sp. nova," and this sheet is taken as the holotype. The senior author has examined all of Handel-Mazzetti's Brassicaceae collections at W and WU, and not one carries the number 1209.

Cardamine fragariifolia is extremely variable in robustness of stem; length of internodes; and leaflet shape, size, apex, margin, and petiole. The variation is continuous, however, and does not fall into any pattern that corresponds with geography. The leaflet margin is serrate or crenate, but in Ludlow & Sherriff 324 (BM) it is deeply so to nearly incised, whereas in Zhou 108309 (IBSC) it is subentire and minutely denticulate.

Status of Loxostemon

All species of Cardamine, including Dentaria L., are characterized by having distinctly margined or narrowly winged replum, elastic fruit dehiscence, and spiral coiling of valves. Except for Loxostemon, this combination of characters is not known elsewhere in the Brassicaceae (Al-Shehbaz, 1988). Nine of the 10 Loxostemon species recognized by Lan and Cheo (1981) and Lan (1987) are endemic to China. Loxostemon pulchellus J. D. Hooker & Thomson, which is the generic type, also grows in Bhutan (Grierson, 1984), India (Hajra and Chowdhery, 1993), and Nepal (Hara, 1979).

Loxostemon was said to differ from Cardamine solely in having expanded instead of slender filaments of the median stamens. All other features of Loxostemon, especially the fruit replum and dehiscence described above, are very common in Cardamine. A critical evaluation of extensive flowering material of Loxostemon, especially from China, shows that the median filaments are distinctly flattened in L. pulchellus, but in the remaining species of Loxostemon they are only slightly flattened or slender, terete, and not expanded at all. Evidently, there is no reliable morphological basis for recognizing Loxostemon as distinct from Cardamine, and the two genera are combined herein following Diels (1912).

Except for L. loxostemonoides (O. E. Schulz) Y. Z. Lan & Y. T. Cheo, the remaining nine species recognized by Lan and Cheo (1981) and Lan (1987) actually represent four species (L. pulchellus, L. delavayi Franchet, L. repens (Franchet) Handel-Mazzetti, and L. smithii O. E. Schulz), of which all except L. pulchellus have names in Cardamine. Handel-Mazzetti (1931) recognized four species in Loxostemon, whereas Hajra and Chowdhery (1993) treated the genus as monotypic. Diels (1912) suggested (p. 205) that L. pulchellus should be placed in Cardamine, although he and subsequent authors never proposed the needed combination. As delimited by Lan and Cheo (1981) and Lan (1987), L. loxostemonoides (O. E. Schulz) Y. Z. Lan & Y. T. Cheo clearly represents three distinct species of Cardamine: C. luxurians (O. E. Schulz) Rashid & H. Ohba, C. loxostemonoides O. E. Schulz, and C. tibetana Rashid & H. Ohba (Rashid and Ohba, 1993).

Cardamine pulchella (J. D. Hooker & Thomson) Al-Shehbaz & G. Yang, comb. nov.

Basionym: Loxostemon pulchellus J. D. Hooker & Thomson, J. Linn. Soc., Bot. 5: 147. 1861. TYPE: "Sikkim graminosis humidis! alt. 10,000--13,000 ped.," J. D. Hooker, s.n. (holotype: K).

Synonyms: Loxostemon incanus R. C. Fang ex T. Y. Cheo & Y. Z. Lan, Bull. Bot. Res. North-East. Forest Inst. 1(3): 52. 1981. Syn. nov. TYPE: China. Yunnan. Chungtien Plateau, 7 July 1930, K. M. Feng 1559 (holotype: KUN, listed as HKA).

Cardamine pulchella is readily distinguished from all of the Himalayan species by its tiny bulbils at the leaf axils. Plants of L. incanus also have bulbils, and they are indistinguishable from those of C. pulchella except for being slightly more pubescent. However, density of the indumentum alone is not a reliable feature for the recognition of infraspecific taxa in Cardamine.

Acknowledgments

We are grateful to George Yatskievych for his critical review of the manuscript and to Henk van der Werff for correcting the Latin. We thank He Se for his translation of some of the herbarium labels. We are grateful to the directors and curators of A, B, BM, CAS, GH, IBSC, K, KUN, MO, NAS, PE, US, W, and WU for the loans of specimens.

LITERATURE CITED

Al-Shehbaz, I. A. 1988. The genera of Arabideae (Cruciferae; Brassicaceae) in the southeastern United States. J. Arnold Arbor. 69: 85--166.

------, G. Yang, L. L. Lou, and T. Y. Cheo. 1998. Delimitation of the Chinese genera Yinshania, Hilliella, and Cochleariella (Brassicaceae). Harvard Papers Bot. 3(1): 79-94.

Cheo, T. Y. 1987. Cardamine. In T. Y. Cheo, ed., Brassicaceae. Fl. Reipubl. Popularis Sin. 33: 184--231. Science Press, Beijing.

Diels, L. 1912. Plantae Chinenses Forrestianae. Notes Roy. Bot. Gard. Edinburgh 5: 161--304.

Grierson, A. J. C. 1984. Cruciferae. In A. J. C. Grierson and D. G. Long, Fl. Bhutan 1(2): 417--445. Royal Botanic Garden, Edinburgh.

Hajra, P. K., and H. J. Chowdhery. 1993. Arabideae. In D. B. Sharma and N. P. Balakrishnan, eds., Fl. India 2: 99--133. Botanical Survey of India, Calcutta.

------, D. M. Verma, and G. S. Giri, eds. 1996. Materials for the flora of Arunachal Pradesh. Vol. 1. Botanical Survey of India, Calcutta.

Handel-Mazzetti, H. 1931. Cruciferae. Symb. Sin. 7: 356--372. Verlag von Julius Springer, Wien.

Hara, H. 1979. Cruciferae. In H. Hara and L. H. J. Williams, eds., An Enumeration of the Flowering Plants of Nepal 2: 38--46. British Museum (Natural History) Publ. 810, London.

Lan, Y. Z. 1987. Loxostemon. In T. Y. Cheo, ed., Brassicaceae. Fl. Reipubl. Popularis Sin. 33: 231--241.

------, and T. Y. Cheo. 1981. Taxa nova generis Loxostemon familiae Cruciferum Sinicarum. Bull. Bot. Res. North-East. Forest Inst. 1(3): 52--58.

Rashid, A., and H. Ohba. 1993. A revision of Cardamine loxostemonoides O. E. Schulz (Cruciferae). J. Jap. Bot. 68: 199--208.

Smith, W. W. 1919. Diagnoses specierum novarum in herbario Horti Regii Botanici Edinburgensis cognitarum CCCCI--CCCCL. Notes Roy. Bot. Gard. Edinburgh 11: 191--232.

Zhang, Y. H. 1986. Hilliella, a new genus of Cruciferae. Acta Bot. Yunnan. 8: 397--406.