Bot. Bull. Acad. Sin. (2000) 41: 237-242

Al-Shehbaz and Peng The genus Barbarea (Brassicaceae) in Taiwan

The genus Barbarea (Brassicaceae) in Taiwan

Ihsan A. Al-Shehbaz1 and Ching-I Peng2,3

1Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299, U.S.A.

2Institute of Botany, Academia Sinica, Nankang, Taipei 115, Taiwan

(Received December 10, 1999; Accepted February 11, 2000)

Abstract. Barbarea R. Brown consists of about 20 species distributed mainly in Europe and Asia, with the native range of one, B. orthoceras Ledeb., extending from central and eastern Asia into North America. In eastern Asia Barbarea is represented by two native species, B. taiwaniana and B. orthoceras, both of which occur in Taiwan. The taxonomy of the Taiwanese species, however, has been the subject of continuous controversy and there are drastically conflicting views as to their limits. The principal reason behind this persistent controversy is a result of the misinterpretation of the limits of two species, one described by Hayata (1913) as Cardamine arisanensis Hayata and the other by Ohwi (1934) as Barbarea taiwaniana Ohwi, by various authors without the examination of type material. We have critically examined all types cited in this paper, and clarified the confusion in the taxonomy of Taiwanese Barbarea. A detailed description of the genus and its species in Taiwan are provided. A key to the species of Barbarea in Taiwan, synonymies, notes on their distribution with maps, and photographs of representative specimens are presented.

Keywords: Barbarea; Barbarea derchiense; Barbarea orthoceras; Barbarea taiwaniana; Brassicaceae; Cruciferae; Distribution; Taiwan; Taxonomy.

Barbarea R. Brown consists of about 20 species distributed mainly in Europe and Asia (Al-Shehbaz, 1988), with the native range of one, B. orthoceras Ledeb., extending from central and eastern Asia into North America (Rollins, 1993). The center of greatest diversity is Turkey and the Balkan Peninsula, where 11 of the 17 species are endemic (Ball, 1993; Coode and Cullen, 1965; Greuter et al., 1986; Tan and Gemici, 1990). Hewson (1982) listed two species as endemic to Australia, but as indicated by Al-Shehbaz (1988) both are somewhat anomalous in Barbarea because of their annual habit and tuberculate, margined or winged seeds.

Barbarea is represented in eastern Asia by two native species, one of which is endemic to Taiwan. The taxonomy of the Taiwanese taxa has been the subject of continuous controversy, however, and there are drastically conflicting views as to their delimitation. Perhaps the principal reason behind this persistent controversy is a result of the fact that the limits of two species, one described by Hayata (1913) as Cardamine arisanensis Hayata and the other by Ohwi (1934) as Barbarea taiwaniana Ohwi, were misinterpreted by various authors without examination of type material. Two of the most recent accounts of the Taiwanese Barbarea, Shen (1996) and Ying (1996) are completely contradictory (see below) and do not provide accurate descriptions of the taxa. A critical re-examination of the problem is therefore necessary. We have examined all types cited in this paper, and we are confident that we have resolved the problems in Taiwanese

Barbarea. A detailed description of the genus based on all of its species worldwide and detailed descriptions of the Taiwanese species are provided.

In his original description of Cardamine arisanensis, Hayata (1913) provided a detailed description and illustrations of the entire plant and cited two syntypes, both of which are deposited at TI and which we critically examined. Hayata did not realize, however, that he was dealing with two species in two different genera. Both syntypes were annotated by Hayata as Cardamine arisanensis Hayata. One syntype, Kawakami & Mori 2252, is a species of Barbarea and consists of a caudex, fragmentary stem, and a few basal leaves, one of which was illustrated accurately in the figure accompanying the original description. For the second syntype, Hayata (1913) wrote only "montibus centralibus, Feb. 1908" in the protologue. The label on the syntype indicates, however, that the plant was collected by Kawakami and Mori (# 3631) on 25 March 1908 (not February) from Ali Shan. Schulz (1903) identified this syntype as Cardamine flexuousa With. subsp. fallax O. E. Schulz. Hayata's (1913) descriptions and illustrations of the cauline leaves, flowers, fruits, and seeds of Cardamine arisanensis were accurately taken from this syntype.

Ohwi (1934) was the first to realize that Hayata (1913) included two species in his original description of Cardamine arisanensis. By listing "Cardamine arisanensis Hayata, Icon. Pl. Formosan. 3 (1913) 20 ex pte., quoad folia" under his original description of B. taiwaniana, Ohwi thereby effectively lectotypified C. arisanensis (lectotype, Kawakami & Mori 3631, TI) and

3Corresponding author. E-mail: bopeng@gate.sinica.edu.tw


Botanical Bulletin of Academia Sinica, Vol. 41, 2000

removed the Barbarea element to his new species. Unfortunately, many workers who dealt with Barbarea in Taiwan (e.g. Liu and Ying 1976; Ying, 1978, 1996; Guo, 1987; Lin, 1993, 1999; Chen, 1998) overlooked this fact, and wrongly interpreted the limits of B. taiwaniana to include what is known elsewhere as B. orthoceras. These authors also mistakenly named the endemic species of Barbarea from Taiwan Cardamine arisanensis or B. arisanensis (Hayata) S. S. Ying. In recent publications on Taiwanese Brassicaceae, only Lu (1977), Shen (1996) and Yang et al. (1997) provided the correct names for the two Taiwanese species of Barbarea. They recognized B. orthoceras var. formosana Kitam. as endemic to Taiwan, however, when in fact this variety is indistinguishable from plants of the highly variable B. orthoceras from other parts of the world. This variety therefore does not merit recognition.

Ying (1995) described Barbarea derchiense S.S. Ying from Taichung Hsien. We have not seen the type, but the detailed description and colored photos clearly indicate that it is not a Barbarea. It is very likely that this species is Brassica rapa L. (including B. campestris L.) because of its entire amplexicaul cauline leaves, rounded (probably misdescribed for globose) seeds, yellow flowers overtopping the flower buds, lyrate basal leaves, and fruits and pedicels to 5 cm long. Cabbages, turnips, cauliflower, and other crops of various species of Brassica are grown in Taiwan, and some are likely to have escaped from cultivation. Liu and Ying (1976), Ying (1996), and Shen (1996) did not mention the genus in their accounts.

Taxonomic Treatment

BARBAREA R. Brown in W. T. Aiton, Hortus Kew. ed. 2. 4: 109. 1812, nom. cons. Type species: B. vulgaris R. Brown

Herbs biennial or perennial with rhizomes or woody caudex, rarely annuals. Trichomes absent or present and unicellular, eglandular, simple. Roots forming a taproot system, sometimes adventitious from lower nodes. Stems erect to ascending, sometimes prostrate, angular, simple or branched basally and/or apically. Basal leaves petiolate, fleshy or not, forming or not forming a rosette, lyrate-pinnatifid or pinnatisect, rarely undivided; terminal lobes larger or rarely subequalling neighboring lateral lobes. Cauline leaves petiolate or sessile, auriculate or amplexicaul at base, entire, dentate, pinnatifid, or pinnatisect, glabrous or basally ciliate. Inflorescences many-flowered, usually dense, ebracteate or very rarely bracteate, terminal, corymbose racemes, elongated slightly or considerably in fruit; rachis straight, or rarely slightly flexuous, striate; bracts when present restricted to lowermost flowers. Fruiting pedicels slender or thickened and nearly as wide as fruit, terete or angled, erect and appressed to rachis, ascending, or divaricate. Sepals oblong to linear, free, deciduous, erect, ascending, or spreading, glabrous or subapically pubescent, somewhat unequal, base of inner pair saccate, margin membranaceous or not. Petals bright to pale yellow, rarely creamy white, erect at base with flaring blade, longer or rarely nearly as long as sepals; blade spatulate

to oblanceolate, apex obtuse to rounded, margin entire; claw short and sometimes obscurely differentiated from blade, glabrous, unappendaged, entire. Stamens 6, only slightly exserted, erect, tetradynamous; filaments filiform, wingless, unappendaged, not dilated at base, glabrous, free; anthers oblong, rounded to sagittate at base, obtuse at apex, not coiled after dehiscence. Pollen tricolpate. Nectar glands 4, median pair toothlike or rod shaped; lateral nectaries semiannular, or annular. Ovules 10-40 per ovary; placentation parietal. Fruit dehiscent, capsular siliques linear or rarely elliptic-linear, terete, 4-angled, or slightly to strongly flattened and latiseptate, appressed to rachis or not, not inflated, sessile or short stipitate, unsegmented; valves papery or leathery, with a prominent midvein and sometimes with obscure or distinct reticulate lateral veins, glabrous or rarely hairy, rounded or rarely keeled, smooth or distinctly torulose, wingless, unappendaged; gynophore to 1 mm long; replum rounded; septum complete, membranous or thickened and papery, sometimes with a distinct midvein; style obsolete, short, or up to 5 mm long, stout to slender, cylindric to subconical, persistent, glabrous; stigma capitate, entire or slightly 2-lobed and lobes free. Seeds 6-20 per locule, uniseriate or subbiseriate, wingless or narrowly winged or margined, oblong, ovoid, or orbicular, plump or slightly flattened; seed coat minutely to coarsely reticulate, rarely tuberculate, not mucilaginous when wetted; cotyledons accumbent, entire.

Key to the Species of Barbarea in Taiwan

1a. Terminal leaf lobe much larger than neighboring lateral lobes; cauline leaves usually lyrate-pinnatifid, with 1-4 lateral lobes; fruit terete-subquadrangular, 1.2-1.5 mm wide; seeds plump, wingless 1. B. orthoceras

1b. Terminal leaf lobe about the same size as neighboring lateral lobes; cauline leaves pinnatisect, with (4-)6-10(-12) lateral lobes; fruit compressed, (1.5-)2-2.5 mm wide; seeds compressed, winged 2. B. taiwaniana

1. Barbarea orthoceras Ledeb., Index Semin. Hort. Dorpat 1824.TYPE: Russia, Baikal, between mouths of Barguzin and Upper Angara rivers, Ledebour s.n. (holotype, LE). s Figure 1

Barbarea orthoceras Ledeb. var. formosana Kitam., Coloured Ill. Herb. Pl. Jap. 2: 179. 1963; Lu, Quart. J. Chin. Forest. 10(3): 97, photo 10. 1977; Shen, J. Exp. Forest, Natl. Chunghsing Univ. 18: 12, fig. 7. 1996; Yang, Liu & Lu, Manual Taiwan Vasc. Pl. 2: 211, photo 535.

Barbarea taiwaniana auct. non Ohwi: Ying, Alpine Pl. Taiwan Color I: 56, photo 54. 1975, Alpine Pl. Taiwan 72, photo 51. 1980; Liu & Ying, Fl. Taiwan 2: 679, pl. 446. 1976; Hsu et al., Alpine Pl. Taiwan 54. 1986; Guo, Fl. Reipubl. Popularis Sin. 33: 248. pl. 65:7. 1987; Lin, Ill. Guide to Taiwan Alpine Pl. 6. 1993, Wild Fl. Taiwan (High elevation) 64. 1999; Chen, Veg. Taiwan 2(2): 450-451. 1997.


Al-Shehbaz and Peng The genus Barbarea (Brassicaceae) in Taiwan

Herbs biennial or perennial. Stems (10-)20-60(-100) cm tall, erect, angled, glabrous throughout. Basal and lowermost cauline leaves petiolate; petiole (0.5-)1-5(-7) cm long, glabrous or rarely ciliate basally; leaf blade (1-)1.5-4(-6) cm long, lyrate-pinnatifid, with (1 or)2-4(-6) lobes on each side of rachis, rarely unlobed, not fleshy; lateral lobes oblong to ovate, 2-10 1-5 mm, entire; terminal lobe considerably larger than lateral ones, 1.5-5 1-2.5 cm. Cauline leaves usually lyrate-pinnatifid, with 1-4 lateral lobes, rarely coarsely toothed, sessile, conspicuously auriculate; auricles ovate to narrowly oblong, to 8 5 mm, ciliate, entire; lateral lobes oblong to ovate, rarely lanceolate, to 2 1 cm, glabrous, entire; terminal lobe much larger than lateral lobes and to 5 3 cm, entire or repand to rarely dentate.

Racemes ebracteate, elongated considerably in fruit. Sepals yellow, oblong, 2.5-3.5 1-1.5 mm, erect, margin scarious, lateral pair slightly saccate. Petals yellow or pale yellow, oblanceolate, rounded, (3-)4-5(-6) 1.5-2 mm, attenuate to base. Filaments yellow, erect, 3-4.5 mm long; anthers oblong, ca. 1 mm long. Fruiting pedicels erect to ascending, (2-)3-6(-7) mm long, terete to subquadrangular, glabrous, stout, slightly narrower than fruit. Fruit linear, (1.5-)2-4(-5) cm 1.2-1.5 mm, terete-subquadrangular, torulose, erect to erect-ascending; gynophore to 0.3 mm; valves with a prominent midrib and lateral veins; style 0.5 -1(-1.2) mm long. Seeds brown, ovate to oblong, 1.2-1.5 0.9-1 mm, uniseriate, somewhat plump, wingless. Flowering June-July; fruiting August-September.

Figure 1. Barbarea orthoceras Ledeb. Photograph of Peng 17360 (HAST) from Taiwan.


Botanical Bulletin of Academia Sinica, Vol. 41, 2000

Additional specimens examined. TAIWAN. TAICHUNG HSIEN: Nanhutashan, Shimada 1408 (TAI), Huang 7817 (TAI), 3,400-3,500 m, Wang 864 (TNM), ca. 3,500 m, Yamazaki et al. 441 (TAI); Hoping, Kenankuan, Wang 2778 (HAST, TNM). NANTOU HSIEN: Jenai, Sunghsuehlo to Tsuifeng, Yang 2219 (TNM), Sunghsuehlow, 31 July 1992, Wang s.n. (TNM), Hohuanshan Military Skiing Training Center, Peng et al. 17360 (HAST, MO, OOM, OSH, S, SAPA, ), Tienchih to Nengkaopeifeng, Chiu et al. 3422 (HAST, TNM), Piluhsi, Lu & Ou 3544 (TAI). CHIAYI HSIEN: Alishan, Kawakami & Mori 10973 (TAIF). HUALIEN HSIEN: Hohuanshan, Kao 7759 (TAI), ca. 3,200 m, Hsieh 950 (TAI), Ou & Kao 9163 (TAI); Nengkaoyueh (Nokogoe), Ohwi 3189 (TNS); Tayuling, ca. 2,565 m, Lai & Liang 13262 (A).

Distribution and Notes. Eastern and central Asia, North America. In Taiwan in the Tsuga-Picea zone, Abies zone or in open grasslands, and on scree, often in moist or wet areas, 2,500-3,500 m (Figure 2).

2. Barbarea taiwaniana Ohwi, Repert. Spec. Nov. Regni Veg. 36: 50. 1934; Masamune, List Vasc. Pl. Taiwan 56. 1954; Lu, Quart. J. Chin. Forest. 10(3): 98, photo 11. 1977; Shen, J. Exp. Forest Natl. Chunghsing Univ. 18: 13, fig. 8. 1996; Yang, Liu & Lu, Manual Taiwan Vasc. Pl. 2: 212, photo 536. 1997. TYPE: Formosa, Mt. Niitaka, July 1933, Jisaburo Ohwi 3677 [holotype, KYO (photo, TNS!); isotype, TNS!]. xWs Figure 3

Cardamine arisanensis Hayata, Icon. Pl. Formosan. 3: 20, ex parte, quoed folia.

Cardamine arisanensis auct. non Hayata: Ying, Alpine Pl. Taiwan Color 1: 56, photo 55. 1975; Liu & Ying, Fl. Taiwan 2: 683. 1976; Cheo, Fl. Reipul. Popularis Sin. 33: 206. 1987.

Barbarea arisanensis (Hayata) S. S. Ying, Alpine Pl. Taiwan Color 2: 170. 1977, Alpine Pl. Taiwan 72, photo 50. 1980, Fl. Taiwan 2nd ed. 2: 749, photo 333, 1996; Hsu et al., Alpine Pl. Taiwan 53. 1986; Lin, Ill. Guide Taiwan Alpine Pl. 4, 1993, Wild Fl. Taiwan (High elevation) 63. 1999; Chen, Veg. Taiwan 2(2): 450-451. 1997.

Herbs perennial. Caudex apically branched or simple in younger plants, often with petiolar remains of previous years. Stems (6-)10-20(-35) cm tall, erect or rarely decumbent when many branched from base, angled, glabrous throughout. Basal and lowermost cauline leaves petiolate; petiole (2-)3-7(-10) cm long, ciliate at least basally, grooved adaxially; leaf blade (2-)3-5(-9) cm long, pinnatisect, with (3-)5-8(-10) lobes on each side of rachis, somewhat fleshy; lateral lobes oblong to ovate, (2-)5-10(-15) (1-)3-6(-10) mm, entire or obtusely lobed; terminal lobe about as large as lateral ones. Cauline leaves pinnatisect, with (4-)6-10 (-12) lateral lobes, petiolate, reduced in size and sessile upward, conspicuously auriculate; auricles ovate to oblong, to 12 5 mm, ciliate, base rounded, entire or rarely toothed; lateral lobes linear to narrowly oblanceolate or oblong , rarely ovate, to 15 5 mm, glabrous, entire or usually lobed or obtusely toothed on proximal margin; ter

Figure 2. Latitudinal and altitudinal distribution maps of Barbarea orthoceras (triangles) and Barbarea taiwaniana (stars) in Taiwan.

minal lobe about as large as neighboring lateral lobes, mostly 3-lobed. Racemes ebracteate, slightly elongated in fruit. Sepals yellowish, usually tinged purple at middle, oblong, 3-4 1-1.5 mm, erect, margin scarious, lateral pair slightly saccate. Petals yellow, oblanceolate, rounded, 5-7 2-2.5 mm, attenuate to base. Filaments yellow, erect, 3-4 mm long; anthers oblong, ca. 1 mm long. Fruiting pedicels erect-ascending, 3-6(-10) mm long, angled to subterete, glabrous. Fruit linear, (1-)1.5-2.5 cm (1.5-)2- 2.5 mm, compressed, somewhat torulose, erect to erect-ascending, somewhat appressed to rachis; gynophore 0.2 -0.5 mm; valves with a prominent midrib; style 0.5-2 mm long. Seeds yellowish brown, ovate to suborbicular, 1.5-2 ca. 1 mm, uniseriate to subbiseriate, somewhat compressed, often winged all around, wing to 0.2 mm wide. Flowering June-July, fruiting August-September.

Additional specimens examined. TAIWAN. HSINCHU HSIEN: Tapachienshan, 20 Jul 1932, Sasaki s.n. (TAI). TAICHUNG HSIEN: Hsuehshan ("Mt. Tugitaka"), Masamune & Susuki 5317 (TAI), Suzuki 5318 (TAI), Aug 1924, Ohashi s.n. (TAIF), Ohashi 28499 (TAIF), Ying 3845, 3894, 3914, 3913, 3915 (all at NTUF), Shu 17 (NTUF), Chiu 1992 (TNM), 3,500-3,884 m, 23 Aug 1995, K. C. Yang s.n. (TAIF), en route from 369-Shanchuang (a lodge) to Hsuehshan peak, 24 Oct 1947, Mori s.n. (TAI), ca. 3,600 m, Hsu & Moore 747 (A, HAST), Yang 5632, 6169 (both at TNM), 369-Shanchuang to Tsueichih, Wang, Huang & Tang 4424 (TAI). NANTOU HSIEN: Yushan National Park, Paiyun Lodge to Yushan main peak, Peng et al. 14384 (HAST, TAIF, TNM), Lu 14799 (TAIF), Paiyun Lodge to Yuanfeng Lodge, Cheng 2327 (TAIF). CHIAYI HSIEN: Yushan ("Mt. Niitaka", "Mt. Morrison"), Kawakami & Mori 2252 (TI), ca. 3,900 m, Hsu 5354 (TAI), Suzuki 13349 (TAI), 3,800-3,900 m, 6 Sep 1960, Kuoh & Tu s.n. (TAI), Chuang 2912 (TAI), Chuang, Kou & Kao 4006 (HAST), Kawakami & Mori 10972 (TAIF), Y. & F. Yamazaki 811 (TI), Ying 1430, 1955, 1975 (all at NTUF), en route from


Al-Shehbaz and Peng The genus Barbarea (Brassicaceae) in Taiwan

Figure 3. Barbarea taiwaniana Ohwi. Photograph of Peng 9549 (HAST) from Taiwan.

Paiyun Lodge to peak, 3,500-3,997 m, Hsu 6274 (TAI), Peng 9549, 14384 (both at HAST), ca. 3,528-3,950 m, Leu 229, 242 (both at HAST), Lu & Ou 3683 (NCUF), en route from Haiunsano to the top of Yushan, Koyama 23900 (TNS), route from summit to Tataka, Tamura, Shimizu & Kao 22134 (TNS), Monroe ("Moroo") Cliff to Tungpu, Hsu 5350 (TAI). TAITUNG HSIEN: Hsiangyangshan, 3,494-3,600 m, Chiu et al. 2909 (HAST, TNM).

Distribution and Notes. Endemic; under Abies, in sunny, rocky areas, above timberline, and in rock crevices; 3,200-3,950 m (Figure 2).

Acknowledgments. We are grateful to Hideaki Ohba (TI) and Shinobu Akiyama (TNS) for the loan of types. We thank Henk van der Werff (MO) for useful comments, Sachiko Nishida (KYO) for the translation of Japanese and Kuo-Fang Chung (HAST) for technical assistance.

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