ISSN 1346-7565 Acta Phytotax. Geobot. 70 (3): 159–172 (2019) doi: 10.18942/apg.201906
Taxonomic Revision of Oxalis subsect. Oxalis (Oxalidaceae)
1,* 2,† 2 Satoshi Aoki , Tetsuo Ohi-Toma and Jin Murata
1Graduate School of Science, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan. *[email protected] (author for correspondence); 2Botanical Gardens, Graduate School of Science, The University of Tokyo, 3-7-1 Hakusan, Bunkyo-ku, Tokyo 112-0001, Japan. † Present address: Nature Fieldwork Center, Okayama University of Science, 1-1 Ridaicho, Kita-ku, Okayama 700-0005, Japan
The classification of Oxalis subsect. Oxalis (Oxalidaceae) is revised based on phylogenetic, cyto- logical and morphological evidence. For the flora of Japan, one new species and one new variety are described, and five new combinations are proposed. The new species, O. nipponica, resembles O. griffithii, but is distinguished by its unique phylogeny, larger genome and distribution. Oxalis nipponica is subdivided into two subspecies, nipponica and kantoensis based on phylogeny and fruit length. Subsp. kantoensis is further divided into two varieties based on ploidy level, length of the fruit and seeds and habitat. While diploids correspond to var. kantoensis, the tetraploids cor- respond to the newly described var. alpigena. Variety alpigena resembles O. acetosella and has been confused with it. Fourteen taxa, including one hybrid, are recognized in subsect. Oxalis.
Key words: new species, new variety, Oxalidaceae, Oxalis nipponica subsp. kantoensis var. alpigena
The taxonomic history of Oxalis L. sect. Ox- cally, have caused frequent misidentifications in alis subsect. Oxalis based on Hara (1954, 1955), subsect. Oxalis, especially of the species in East- Terao (1979), Huang & Liu (2003), Huang et al. ern Asia (Liu & Watson 2008). (1998), Lourteig (2000), Amano (2001), and Liu To reassess the taxonomy of subsect. Oxalis, & Watson (2008) was summarized previously we compared the morphology, genome size and (see Table 1 in Aoki et al. 2017). In the Flora of molecular phylogeny of samples of Oxalis from a Japan (Amano 2001), this section was treated as wide geographical area (Aoki et al. 2017, 2018). sect. Acetosellae (Reiche 1894) R. Knuth 1914, In the phylogenetic tree (Fig. 1), some taxa were but it should have been sect. Oxalis, because this not monophyletic. section includes O. acetosella L., the type of the In our studies, Oxalis griffithii var. griffithiiin genus Oxalis (Turland et al. 2018, International Japan (including the indistinguishable O. aceto- Code of Nomenclature Art. 22.1). Lourteig (2000) sella var. longicapsula) formed a clade (Clade C) treated all taxa in the subsection and recognized independent of those in China (Clade A). Oxalis O. magellanica G. Forst. in Oceania and South acetosella var. longicapsula was also in Clade C, America, O. griffithiiEdgew. & Hook.f., O. obtri- and O. griffithii var. kantoensis was placed in angulata Maxim. and O. leucolepis Diels in the Clade D. Most Japanese plants of O. acetosella Far East and eastern Asia, O. oregana Nutt. ex var. acetosella, formed a clade with O. acetosella Torr. & A. Gray and O. trilliifolia Hook. in North var. acetosella in China and Europe (Clade B), America and the widespread O. acetosella. Leaf- but a few Japanese plants were in Clade D. Addi- let shape and the spacing of the petioles on the tionally, the American O. acetosella var. aceto- rhizome, which are difficult to express numeri- sella occupied a unique phylogenetic position (as 160 Acta Phytotax. Geobot. Vol. 70
Oxalis montana in Fig. 1). The comparison be- In the present taxonomic treatment, we made tween the previous classification (Lourteig 2000, species correspond to the confident clades. Intra- Amano 2001) and the results from our analysis is specific taxa were assigned based on cytological summarized in Table 1. or minor phylogenetic differences accompanied Our cytological analysis showed differences by their ecological and/or morphological differ- in genome size among Clades A–D, but Clades C ences. By minor phylogenetic differences, we and D had genomes of nearly the same size. mean monophyly with low confidence or mono- Clades C and D also had genomes of two sizes, typic lineages that render a species paraphyletic which corresponded to the diploids and tetra- or polyphyletic if they are considered as species. ploids reported by Terao (1979). We examined specimens in the herbaria of Kyoto Besides examining specimens, we measured University (KYO), Tokyo Metropolitan Univer- the length of the capsule, the length to width ratio sity (MAK), Makino Botanical Garden (MBK), of the capsules and the length of seeds among our National Taiwan University (TAI), Hokkaido samples. We then compared the measurements. University Museum (SAPS), and the University From the data gathered from samples of O. of Tokyo (TI). We also consulted digital images griffithii subsp. griffithii, we could not distin- of specimens at the herbaria BR, E, G-DC, GH, guish between the samples from China (Clade A) HPSU, ID, K, LINN, M, P, PE, SOC, SRP, TNS, and Japan (Clade C). While diploids and tetra- US and WTU. The herbarium acronyms follow ploids in Clade C were indistinguishable, capsule Thiers (2018). length and seed length were informative for dis- From our results, we recognize two new cryp- tinguishing between diploids and tetraploids in tic taxa. We treated the Japanese plants previous- Clade D. Consequently, we decided to revise sub- ly identified as O. griffithii var. griffithii as a new section Oxalis. In this revision, we excluded O. species, O. nipponica subsp. nipponica. Our magellanica, because it was located phylogeneti- treatment is based on differences in genome size cally outside the outgroup in our phylogenetic and phylogenetic position. analysis (Aoki et al. 2017). We kept the descrip- The second unrecognized cryptic taxon cor- tion of North American taxa simple, because we responds to tetraploids of O. griffithii var. kan- examined few specimens in our previous studies toensis (Terao) T. Shimizu. This cryptic taxon (Aoki et al. 2017, 2018). was previously treated as tetraploids of O. aceto- Oxalis japonica Franch. & Sav. has been con- sella by Terao (1979). In a previous study (Aoki et sidered to be a Japanese endemic distinct from O. al. 2017), we determined its phylogenetic position griffithii (cf. Makino 1908, Hara 1954), probably and ploidy level. Considering its characteristic based on the description and the Japanese name habitat and distribution, we now chose to treat used in the original study. Hara (1955), however, this tetraploid as a new variety distinct from var. determined the holotype, Savatier 2816 (P, kantoensis and from O. acetosella, despite the P00724040) of O. japonica, to be O. martiana difficulty in separating them based on morpholo- Zucc., which had been introduced to Japan from gy. The diploid plant previously identified as O. South America. Hara (1955) identified the Japa- griffithii var. kantoensis is now treated as O. nip- nese plants that had been treated as O. japonica ponica subsp. kantoensis var. kantoensis, and the or O. acetosella subsp. japonica (Franch. & Sav.) cryptic tetraploid is treated as O. nipponica sub- H. Hara as O. griffithii. Huang et al. (1998) ac- sp. kantoensis var. alpigena. We also treat O. cepted O. acetosella subsp. japonica and synony- wulingensis from China, O. acetosella subsp. mized O. obtriangulata under it without consid- griffithiivar. formosana from Taiwan, and O. tai- ering Hara’s (1955) treatment. In addition, they monii from Taiwan as subspecies of O. griffithii. (Huang et al., 1998) did not recognize O. aceto- We treated them as subspecies, since all of them sella subsp. griffithii as occurring in Japan. In were included in the same clade as O. griffithii this study, we follow the treatment of Hara (1955). (Clade A), but did not share identical sequences October 2019 Aoki & al. – Taxonomic Revision of subsect. Oxalis 161
Table 1. Comparison between previous taxonomy (Lourteig 2000, Amano 2001) and taxonomy proposed here for confusing taxa in subsect. Oxalis. Proposed taxonomy shows scientific names suggested in this article and their corresponding phy- logenetic position as shown in Fig. 1 and ploidy levels for taxa in Clade D.
Previously recognized taxa Proposed taxa O. griffithii (Clade A) O. griffithii var. griffithii O. nipponica subsp. nipponica (Clade C) O. griffithii var. kantoensis (diploid) O. nipponica subsp. kantoensis var. kantoensis (Clade D, diploid) O. acetosella (Clade B, diploid) O. acetosella var. acetosella (diploid, tetraploid) O. montana O. nipponica subsp. kantoensis var. alpigena (Clade D, tetraploid) O. acetosella var. longicapsula O. nipponica subsp. nipponica (Clade C)
Fig. 1. Abridged phylogeny of Oxalis subsect. Oxalis based on nuclear ribosomal internal transcribed spacer (ITS) and Bayes- ian methods. Numbers near branches indicate posterior probabilities and bootstrap values by maximum likelihood and maximum parsimony methods. Hyphens indicate branches that did not appear in analysis; branches without numbers are monotypic branches based on a single sequence. For details, see Aoki et al. (2018).
with Oxalis griffithii subsp. griffithii, and they cluding one hybrid, in subsect. Oxalis: O. aceto- exhibited clear morphological differences from sella, O. obtriangulata, O. nipponica subsp. nip- subsp. griffithii. We also recognize O. montana as ponica, O. nipponica subsp. kantoensis var. kan- distinct from O. acetosella based on its phyloge- toensis, O. nipponica subsp. kantoensis var. alpi- netic position. gena, and O. acetosella × O. nipponica. Our revision recognizes six taxa in Japan, in- 162 Acta Phytotax. Geobot. Vol. 70
Taxonomic Treatment
Key to taxa of Oxalis sect. Oxalis subsect. Oxalis in Eastern Asia and surrounding regions.
1a. Leaflets longer than their wide ...... 2 1b. Leaflets wider than their long ...... 3 2a. Lateral leaflets arranged at 90° angle from petioles ...... 4b. O. griffithii subsp. wulingensis 2b. Lateral leaflets arranged at 120° angle from petioles ...... 4c. O. griffithii subsp. taimonii 3a. Petals with dark purple spots at base; rhizome including scales less than ca. 2 mm thick ...... 2. O. leucolepis 3b. Petals without purple spots; rhizome including scales more than 3 mm thick ...... 4 4a. Apex of leaflet truncate; peduncle shorter than petiole at maturity of capsule ...... 3. O. obtriangulata 4b. Apex of leaflet rounded or obtuse; peduncle longer than petiole at maturity of capsule ...... 5 5a. Capsules oblong (more than twice as long as wide) ...... 6 5b. Capsules globular (less than twice as long as wide) ...... 7 6a. ITS sequence containing GTGGTTG, GCCTTTG, AAAAAAA, CACAATC, GGCCGAG, TTGTTGC, TTTGAAA, TGGTCTC, TCTTGAG, and CTTTGCC; plants of continental Asia (China, India, Bhutan, and Nepal) ...... 4a. O. griffithii subsp. griffithii 6b. ITS sequence containing GTGTTTG, GCCTTGG, AAATAAA, CACGATC, GGCGGAG, TCGTTGC, TTTAAAA, TGGTCTC, TCTCGAG, and CTTCGCC; plants of Japan ...... 5a. O. nipponica subsp. nipponica 7a. Seeds more than 2.5 mm long, usually 3 or more mm long ...... 8 7b. Seeds less than 2.7 mm long, usually 2.5 mm or less long ...... 9 8a. Capsules 4.1–8.3 mm long, ca. 6.7 mm on average; seeds 2.8–3.8 mm long, ca. 3.2 mm on average; diploid ...... 5b-I. O. nipponica subsp. kantoensis var. kantoensis 8b. Capsules 3.5–7.3 mm long, ca. 4.9 mm on average; seeds 2.0–3.3 mm long, ca. 2.8 mm on average; tetraploid ...... 5b-II. O. nipponica subsp. kantoensis var. alpigena 9a. Leaflets obcordate ...... 1. O. acetosella 9b. Leaflets obtriangular, angles sometimes protruding ...... 4d. O. griffithiisubsp. formosana
1. Oxalis acetosella L., Sp. Pl. 1: 433. 1753. — pan, Hokkaido: Chatsu, Isl. Okushiri, M. Tatewa- Type: No information on the specimen [lecto- ki s.n. (holo- SAPS 21300 digital image!). LINN 600.7 designated by Nasir (1971); digital = O. parviflora Lej., Fl. Spa. 307. 1813. ≡ O. image!]. acetosella var. parviflora (Lej.) DC., Prodr. 1: = Oxalis acetosella L. var. caerulea DC., Pro- 700. 1824. – Type: Belgium, circa Verviam & dr. 1: 700. 1824. – Type: Not found. Malmundarum, A. Lejeune s.n. (lecto- BR = O. acetosella L. var. lilacina Lange., 0000012172511 digital image!). Haandb. Danske fl. 395. 1851. – Type: Not desig- = O. taquetii R. Knuth in Notizbl. Bot. Gart. nated. Berlin-Dahlem. 308. 1919. – Type: Korea, E. J. = O. acetosella L. var. purpurea Lej., Fl. Spa. Taquet 613 (syn- E 00326129 digital image!). 307, 337. 1813. – Type: Not designated. = O. vulgaris Gray, Nat. Arr. Brit. Pl. 630. = O. acetosella L. var. purpurascens H. Mart., 1821. – Type: Not designated. Prodr. fl. mosq. 81. 1817. Type: Belgium, A. = O. vulgaris Gray var. caerulea Gray, Nat. Lejeune s.n. (lecto- BR 0000012172368 digital Arr. Brit. Pl. 630. 1821. – Type: Not designated. image!). = O. acetosella L. var. rosea Peterm. in Fl. Herbs, perennial, winter green. Rhizomes elon- Lips. Excurs. 506. 1838. – Type: Not designated. gate, covered with scale leaves and bases of peti- = O. acetosella L. var. subpurpurascente DC., oles. Scale-like leaves triangular, sericeous when Prodr. 1: 700. 1824. – Type: Not found. young. Base of petiole scaly, triangular, and seri- = O. acetosella L. var. vegeta Tatew. in Trans. ceous when young, abscission layer round. Leaf- Sapporo Nat. Hist. Soc. 16: 86. 1940. – Type: Ja- lets obcordate, ciliate; longest vein of terminal October 2019 Aoki & al. – Taxonomic Revision of subsect. Oxalis 163 leaflet ca. 5–25 mm long; both surfaces pubes- lectotype [“Habitat in Virginia.” lecto- LINN cent, abaxial surface whitish green, purple or red. 600.11, P00724040 digital image! designated by Flowers solitary; peduncle and pedicel much lon- Reveal (2007)] could not be identified as O. ace- ger than petiole at maturity of capsule, pubescent, tosella or any of its allies based on its long, naked pedicel densely pubescent; bract apparently 1, pedicel above the bracts and long petals. (3) Ox- acute to deeply emarginate, abaxial surface with alis acetosella var. violacea Westf. was also ac- 2 lines of dense hairs; sepals 5, ciliate, lanceolate, cepted by Knuth (1930), but we have not verified green or reddish, abaxial face pubescent; petals the original literature. (4) We did not confirm the five, lanceolate, emarginate, white or rarely pink, type specimens of O. acetosella var. caerulea sometimes blue when dried, always with yellow and O. acetosella var. subpurpurascente. spots at base, veins sometimes pink or purple Concerning the Japanese plants, the tetra- from base to margin; stamens 10, dimorphic: 5 ploids of O. acetosella reported by Terao (1979) longer and 5 shorter arranged alternately; anthers belong to another taxon as noted above. We syn- cream colored, with 2 locules arranged inward onymize O. acetosella var. longicapsula under O. when immature, outward at maturity; filaments nipponica subsp. nipponica based on the results white, translucent; pistils 5; stigmas yellow, of our phylogenetic analysis (Aoki et al. 2017). translucent, twisted, uneven; styles white, trans- lucent, smooth; ovary green; ovules 1 or 2 per Representative specimens examined. Japan. Nagano locule. Capsule green, globular, sometimes spot- Pref., Shinshu: Shinshu Komagatake, 2 August 1880, col- lector unknown s.n. (TI). Tochigi: Nikko, 18 June 1878, ted red, opening at maturity, ca. 4–6.7 mm long. collector unknown s.n. (TI). Nikko, 29 June 1878, G. K. Seeds covered with white translucent membrane s.n. (TI). Nikko Futaara yama, 12 June 1878, collector un- when immature, turning brown and darken in known s.n. (TI). South Korea. Gangwon: Mt. Hambeak, age, asymmetrically ovoid, longitudinally ridged, H. T. Im s.n., H. T. Im s.n. Switzerland. Kt. St. Gallen, E ca. 1.7–2.7 mm long. Chasmogamous flowers of St. Gallen-St. Fiden, 26 April 1980, E. Zogg 4518 (TAI). from spring to early summer. Cleistogamous flowers from early summer to late autumn, few in midsummer. 2. Oxalis leucolepis Diels in Notes Roy. Bot. Gard. Edinburgh 5: 223–224. 1912. Distribution. Japan, Sakhalin, Kuril Islands, ≡ O. acetosella L. subsp. leucolepis (Diels) C. Eurasia (temperate to subarctic region), Great Brit- C. Huang & L. R. Xu in Fl. Reipubl. Popularis ain, Ireland, Iceland (?) and northern Africa (?). Sin. 43: 9. 1998. – Type: China, W. Yunnan, G. Forrest 4287 (holo- K 000692014 digital image!), Habitat. Shady environments and on level G. Forrest 4287 (iso- E 00327127 digital image!; ground, moss-covered rocks and fallen trees. P 00724045 digital image!; IBSC 000803 digital Plants on rocks and fallen trees tend to be small- image!). er, hence, variable in size. Oxalis leucolepis is similar to O. acetosella in leaf shape, but is distinguished by the much thinner rhizomes with Japanese name. Komiyama-katabami. fewer scales. The scale leaves are covered with very short hairs, hence glabrous to the naked eye. The petals are Notes. Lourteig (2000) cited several syn- clearly different: the base of the petals of O. leucolepis has purple spots and purple veins; O. acetosella has yel- onyms of O. acetosella and their types. We com- low spots. ment on some of them as follows: (1) we treat O. montana Raf. (= O. americana Bigelow) as a dis- Rhizomes elongate; scale leaves sparse, triangu- tinct species because our previous study (Aoki et lar, pilose when young. Leaflets obcordate, al. 2017) showed its unique phylogenetic position sparsely ciliate. Flower solitary; petals white, (see below). (2) Oxalis longifloraL. should be as- purple spot at base and purple veins from base to signed to other than subsect. Oxalis because its middle. 164 Acta Phytotax. Geobot. Vol. 70
Distribution. China (south), India (north), Leaflets emarginate; Flower solitary; peduncle Bhutan, and Nepal. and pedicel pubescent; bract apparently 1, trun- cate to emarginate; sepals 5, lanceolate, green or Representative specimens examined. China. Hubei: reddish; petals 5, lanceolate, emarginate; stamens Shennongjia, 8 August 2015, S. Aoki 420 (TI). 10, dimorphic, longer 5 and shorter five arranged alternately; anthers with 2 locules; pistils 5; cap- 3. Oxalis obtriangulata Maxim. in Mélanges sules opening at maturity. Biol. Bull. Phys.-Math. Acad. Imp. Sci. Saint-Pé- tersbourg 6: 260. 1867. – Type: Russia, Primor- Notes. Oxalis griffithii corresponds to Clade sky, Posyet Bay along wooded near post, K. Max- A (Fig. 1), which is well supported with 1.00 pos- imowicz (lecto- LE designated by Tzvelev 1988 in terior probability in the Bayesian method, and 94 Russian; syn- P 00724047 digital image!; syn- P and 90 bootstrap values in the maximum likeli- 00724048 digital image!; syn- K 000692015 digi- hood (ML) method and maximum parsimony tal image!; syn- L 0018241 digital image!; syn- (MP) method. Except for the nominative subspe- GH 00241909 digital image!; syn- US 00101067 cies, we recognize three subspecies within this digital image!; syn- M 0172323 digital image!). clade based on their phylogenetic uniqueness and ≡ O. japonica Franch. et Sav. var. obtriangu- morphology. lata (Maxim.) Makino, Ill. Fl. Jap. 400. 1940.
Herbs, perennial, deciduous. Rhizomes with 4a. subsp. griffithii dense scale leaves. Scale-like leaves triangular, ≡ O. leucolepis Diels var. griffithii (Edgew. & pubescent when young. Leaflets ciliate, obtrian- Hook.f.) R.C. Srivast. in Novon 8: 203. 1998. ≡ O. gular, truncate but slightly emarginate; both sur- acetosella L. subsp. griffithii (Edgew. & Hook.f.) faces pubescent, abaxial surface whitish green, H. Hara in J. Jap. Bot. 30: 22. 1955. purple or red. Flower solitary; petals white, with = O. hupehensis R. Knuth in Notizbl. Bot. purple veins from base to middle; peduncle pu- Gart. Berlin-Dahlem 7: 308. 1919. – Type: China, bescent, pedicel densely pubescent; sepals 2, lin- Hubei, Patung [Badong], E. H. Wilson 264 (syn- ear. Capsule green, oblong. Seeds asymmetrical, P 00724042 digital image!; syn- US 00664174 ovoid, longitudinally ridged, ca. 2.5 mm long. digital image!; syn- E 00327135 digital image!). Chasmogamous flowers in spring. Cleistogamous flowers in early summer. Herbs, perennial. Rhizomes sometimes elongate, with scale leaves and bases of petioles. Scale-like Distribution. China (Northeastern region), leaves triangular to lanceolate, sericeous when Korea, Japan, Russian Far East. young. Base of petiole scaly, triangular to oblong, and silky when young, abscission layer round, Japanese name. Ooyama-katabami. sometimes with 2 filmy or triangular appendages on margin. Leaflets ciliate, obtriangular; longest Representative specimens examined. Japan. Nagano: vein of terminal leaflet ca. 8–17 mm long; both Karuizawa, 27 April 2014, S. Aoki 34 (TI). Gunma: Mt. Narukami, 30 July 2014, S. Aoki 73 (TI). South Korea. surfaces pubescent. Peduncle and pedicel much Gangwon: Mt. Maekun, 29 June 2014, H. T. Im 106071 longer than petiole at maturity of capsule; bracts (TI). truncate to emarginate, abaxial surface with 2 lines of dense hairs; sepals ciliate, green or red- dish, abaxially pubescent; petals usually white 4. Oxalis griffithii Edgew. & Hook.f., Fl. Brit. with yellow spots at base or sometimes with pink India 1: 436. 1872. – Type: Bhutan, Griffith 607 or purple veins from base to margin; anthers [lecto- K 000692016 digital image! designated by cream colored, arranged introrse before maturity, Hara (1955) as holo-]. extrorse at maturity; filaments white, translucent; October 2019 Aoki & al. – Taxonomic Revision of subsect. Oxalis 165 stigmas yellow, translucent, twisted, uneven; Distribution. Endemic to alpine Taiwan. styles white, purple or pink, translucent, equal in length; ovary green, ovule 1 or 2 per locule. Cap- Japanese name. Senzan-katabami. sule oblong, ca. 5.5–12.7 mm long. Seeds covered with white translucent membrane when imma- Notes. Oxalis taimoni was named for the col- ture, turning brown and darkening with age, lector, Taimon Ito, and misspelled as “Oxalis tae- asymmetrical, ovoid, longitudinally ridged, ca. moni” by Huang and Huang (1990). Here, we cor- 2.4–3.8 mm long. Chasmogamous flowers in rect the Latin termination of the original spelling spring. Cleistogamous flowers from early sum- [International Code of Nomenclature Art. 60.8 mer to late autumn, few in midsummer. (Turland et al. 2018)].
Distribution. China, India, Bhutan, and Nepal. Representative specimens examined. Taiwan. Taic- hung: 369-shan-chung to Tsue-chih, Hsuehshan, J. C. Specimens examined. China. Sichuan: Mt. Emei, S. Wang, S. F. Huang & W. S. Tang s.n. (TAI216849). Taic- Aoki 79, March 2017 (TI). hung: 369-shan-chung to Tsue-chih, Hsuehshan, J. C. Wang, S. F. Huang & W. S. Tang s.n. (TAI216844). Taic- hun: 369-shan-chung to Tsue-chih, Hsuehshan, J. C. Wang, S. F. Huang & W. S. Tang s.n. (TAI216846). 4b. subsp. wulingensis (T. Deng, D. G. Zhang & Z. L. Nie) S. Aoki & J. Murata, comb. & stat. nov. 4d. subsp. formosana (Terao) S. Aoki & Basionym: O. wulingensis T. Deng, D. G. J. Murata, comb. nov. Zhang & Z. L. Nie in Syst. Bot. 38: 156. 2013. – Basionym: O. acetosella L. subsp. formosana Type: China, Hunan: Sangzhi, Badagongshan Terao in Acta Phytotax. Geobot. 30: 61. 1979. ≡ National Nature Reserve, 2 April 2007, Deng, O. acetosella L. subsp. griffithii var. formosana Zhang & Nie 544 (holo- KUN; iso- PE 2452701 (Terao) S. F. Huang & T. C. Huang in Taiwania digital image!). 35: 10. 1990. – Type: Taiwan, Alishan, 2 April 1977, K. Inoue & M. Sugiyama s.n. (holo- TI!). Rhizomes covered with base of petioles. Leaflets oblong, retuse, lateral leaflets arranged at 90° an- Rhizomes sometimes elongate, covered with gle from petiole; petals pink with lilac veins. scale leaves and bases of petioles. Scale-like Capsule oblong. leaves sericeous when young. Base of petiole scaly, triangular to oblong, sericeous when Distribution. Endemic to China (Hubei and young, abscission layer round. Leaflets ciliate, Hunan). obtriangular, emarginate; longest vein of termi- nal leaflet ca. 6–12 mm long; both surfaces pu- bescent. Peduncle and pedicel much longer than 4c. subsp. taimonii (Yamam.) S. Aoki & petioles at maturity of capsule; bracts truncate to J. Murata, comb. nov. emarginate, abaxial surface with 2 lines of dense Basionym: O. taimonii Yamam. in J. Soc. hairs; sepals ciliate, abaxially pubescent; petals Torp. Agric. 4: 51–52. 1932. (as “taimoni”) ≡ O. white, rarely pink, with yellow spots at base; an- acetosella L. subsp. taemonii (Yamam.) S. F. thers cream colored, introrse when immature, ex- Huang & T. C. Huang in Taiwania 35: 10. 1990. trorse at maturity; filaments white, translucent; – Type: Taiwan, mont. Taihasenzan, , T. Ito s.n. stigmas yellow, translucent, twisted, uneven; (holo- TAI 118905!). styles white, translucent, smooth; ovary green; ovule(s) 1 or 2 per locule. Capsule green, globu- Rhizomes sparsely covered with base of petioles. lar, ca. 4.1–6.7 mm long. Seeds covered with Leaflets emarginate, obcordate, slightly longer white and translucent membrane when immature, than wide. Capsules globular. asymmetrical, ovoid, longitudinally ridged, ca. 166 Acta Phytotax. Geobot. Vol. 70
1.9–2.8 mm long. low, translucent, twisted, uneven; styles white, rarely pink and translucent, equal in length; ova- Distribution. Taiwan and the Philippines (Lu- ry green. Capsules green, sometimes spotted red, zon Island). open at maturity. Seeds covered with white trans- lucent membrane when immature, brown and Japanese name. Arisan-katabami. darkening in age, asymmetrical, ovoid, longitudi- nally ridged. Chasmogamous flowers spring to Representative specimens examined. Taiwan. Taitou: early summer. Cleistogamous flowers early sum- Heitou douro, T. Hosokawa 5352 (TAI064309). Kwaren: Nankotaizan, T. Suzuki, N. Hukuyama & H. Simada mer to late autumn, few in midsummer. ST17586 (TAI064305). Kagi: Mt. Ali, S. Sasaki s.n. (TAI064302). Taihoku: Bunzangun, Babo Kuru, T. Suzuki & Distribution. Endemic to Japan. T. Nakamura ST183361 (TAI116801). Etymology. From the pronunciation of the name of the country, Nippon, in Japanese, where 5. Oxalis nipponica S. Aoki & J. Murata, sp. nov. it is endemic. The specific epithet, japonica, is Oxalis nipponica cannot be distinguished from O. preoccupied by O. japonica Franch. & Sav. griffithii subsp. griffithii morphologically, but it has a ge- nome ca. 27 % larger than O. griffithiisubsp. griffithiiand Notes. Monophyly of Oxalis nipponica was a unique phylogenetic position according to Aoki et al. well supported with 1.00 posterior probability in (2017). the Bayesian analysis, and 82 and 93 bootstrap Typus. Japan, Mie: Miyazumakyo, 17 April 2015, S. values in ML and MP methods, but was divided Aoki 145 (holo- TI!). into two clades (C & D in Fig. 1) (Aoki et al. [O. acetosella L. var. japonica (Franch. & 2017). The plants in the two clades can be distin- Sav.) Makino in Bot. Mag. (Tokyo) 22: 171. 1908, guished by the morphology of their capsules, but pro parte excl. typ.] the confidence of Clade D is not strong (0.94 pos- [O. acetosella L. subsp. japonica (Franch. & terior probability, and 67 and 73 bootstrap values Sav.) H. Hara in J. Fac. Sci. Univ. Tokyo, Sect. 3, in ML and MP methods). Because of this uncer- Bot. 6: 82. 1952, pro parte excl. typ.] tainty, we treat the plants of Clade D as a subspe- [O. acetosella L. subsp. japonica (Franch. & cies of O. nipponica rather than as a distinct spe- Sav.) H. Hara, Enum. Sperm. Jap. 3: 8. 1954, pro cies. parte excl. typ.]
Herbs, perennial. Rhizomes covered with scale- 5a. subsp. nipponica —Fig. 2. like leaves and base of petioles. Scale-like leaves [O. acetosella L. var. japonica (Franch. & triangular to lanceolate, silky when young. Base Sav.) Makino f. japonica Makino, Bot. Mag. (To- of petiole oblong, silky when young, abscission kyo) 22: 171. 1908, pro parte excl. typ.] layer round, sometimes with 2 filmy or triangular = O. acetosella L. var. japonica (Franch. & appendages on margin. Leaflets obtriangular, Sav.) Makino f. rubriflora Makino in Bot. Mag. emarginate, ciliate; both surfaces pubescent, ab- (Tokyo) 22: 171. 1908. ≡ O. acetosella L. subsp. axial surface whitish green, purple or red. Flower griffithiiEdgew. & Hook.f. f. rubriflora (Makino) solitary; peduncle and pedicel much longer than Terao in Acta Phytotax. Geobot. 30: 61. 1979. ≡ petioles at maturity of capsule, pubescent, pedi- O. griffithii Edgew. & Hook.f. f. rubriflora cel densely pubescent above bracts; petals 5, lan- (Makino) Sugim. ex Yonek. in J. Jap. Bot. 86: ceolate, emarginate; stamens 10, dimorphic: lon- 234. – Type: unknown. ger 5 and shorter 5 arranged alternately; anthers = O. acetosella L. var. longicapsula Terao in cream colored, with 2 locules, introrse before ma- Acta Phytotax. Geobot. 30: 59. 1979. – Type: Ja- turity, extrorse at maturity; pistils 5; stigmas yel- pan, Iwate: near Fuenuki-no-taki, 13 August October 2019 Aoki & al. – Taxonomic Revision of subsect. Oxalis 167
1976, H. Terao 328 (holo- KYO!). Representative specimens examined. Japan. Suou: = O. acetosella var. longicapsula f. rosea Kisiki, Kisiki village, 23 October 1892, J. Nikai s.n. (TI). Terao in Acta Phytotax. Geobot. 30: 60. 1979. – Kishu: Mt. Koya, 18 July 1883, collector unknown s.n. (TI). Aomori: Zatouishi, collector unknown s.n. Type: Japan, Fukushima: Yama-gun, Kitashioba- (MAK72707). Gifu: Sasagadake, M. Matsui s.n. ra-mura, Y. Baba s.n. (holo- TNS 181261 digital (MAK72607). Kyoto: Tanba, S. Takami s.n. (MAK72615). image!). Hokkaido: Hiyama, Kaminokunimura, Yunotai, M. Hara s.n. (KYO). Herbs, winter green. Rhizomes sometimes elon- gate. Longest vein of terminal leaflet ca. 7–30 mm long; bract apparently1, rarely 2. When 1, 5b. subsp. kantoensis (Terao) S. Aoki & acute to bifid (liner when 2), abaxial surface with J. Murata, comb. & stat. nov. 2 lines of dense hairs. Sepals 5, ciliate, lanceo- Basionym: O. acetosella L. subsp. griffithii late, green or reddish, abaxial face pubescent; (Edgew. & Hook.f.) H. Hara var. kantoensis Terao petals white or sometimes pink, sometimes blue in Acta Phytotax. Geobot. 30: 62. 1979. ≡ O. when dried, sometimes with yellow spots at base. griffithii Edgew. & Hook.f. var. kantoensis Capsule oblong, ca. 6.4–16.5 mm long. Seeds ca. (Terao) T. Shimizu in J. Phyotogeogr. Tax. 37: 2.5–3.9 mm long. Diploids and tetraploids. 120. 1989. – Type: Japan, Tokyo: Mt. Takao, 17 June 1977, H. Terao 354 (holo- KYO!). Distribution. Endemic to Japan. Honshu (excl. Kanto region, Shizuoka Pref. and Yamanashi Leaflets: adaxial surface sparsely pubescent or Pref.), Sado Island, Oki Island and Hokkaido glabrous, abaxial surface pubescent, whitish (southern part). green, purple or red. Bract apparently 1, truncate to bifid, abaxial surface with 2 lines of dense Habitat. Oxalis nipponica subsp nipponica hairs; sepals lanceolate, green, ciliate, abaxial occurs from sea level to ca. 1,600 m. It prefers surface pubescent; petals white; anthers cream shady, wet environments, such as riverside for- colored, locules 2; filaments white, translucent; ests and valley lines within forests. It is usually styles white, translucent, equal in length. Cap- on the ground and rarely on rocks and fallen sules oblong. trees. Distribution. Japan (Kanto region, Shizuoka Japanese name. Miyama-katabami. Pref., Shikoku District, and Kyusyu District to Yakushima). Notes. Oxalis nipponica can be recognized only by genome size and molecular analysis. It Notes. Oxalis nipponica subsp. nipponica cannot be distinguished morphologically from O. comprises Clade D (Fig. 1), has diploid and tetra- griffithiisubsp. griffithii, which does not occur in ploid individuals. The two ploidy levels differ in Japan. morphology, habitat and distribution. The dip- No specimens were cited in the original de- loids correspond to O. griffithii var. kantoensis scription of O. acetosella var. japonica f. rubri- (Terao) T. Shimizu while the tetraploids corre- flora, and no plausible original material was spond to plants that Terao (1979) reported to be found in TI, MAK or MBK. tetraploids of O. acetosella var. acetosella. The Clade C (Fig. 1) included a sample from the type locality of O. acetosella var. longicap- sula. We were unable to distinguish that variety 5b-I. var. kantoensis (Terao) S. Aoki & morphologically, hence we treat O. acetosella J. Murata, comb. nov. var. longicapsula as a synonym of O. nipponica Basionym: O. acetosella L. subsp. griffithii subsp. nipponica. (Edgew. & Hook.f.) H. Hara var. kantoensis Terao 168 Acta Phytotax. Geobot. Vol. 70 in Acta Phytotax. Geobot. 30: 62. 1979. ≡ O. yellow spot at base. Capsules ca. 3.5–7.3 mm griffithii Edgew. & Hook.f. var. kantoensis long. Seeds ca. 2–3.3 mm long. (Terao) T. Shimizu in J. Phytogeogr. Tax. 37: 120. 1989. Distribution. Japan (western Shizuoka pref., [O. acetosella L. var. japonica (Franch. & Shikoku region and southern Kyusyu region, in- Sav.) Makino f. japonica Makino in Bot. Mag. cluding Yakushima). (Tokyo) 22: 171. 1908, pro parte excl. typ.] Habitat. Oxalis nipponica var. alpigena oc- Herbs, winter dormant. Rhizomes sometimes curs at relatively higher elevations (ca. 1,000 m) elongate. Longest vein of terminal leaflet ca. than the diploid, var. kantoensis, and prefers 9–20 mm long; Petals sometimes with yellow shady environments. spots at base. Capsules ca. 4.1–8.3 mm long. Seeds ca. 2.8–3.8 mm long. Etymology. The epithet, alpigena, from the habitat at higher elevations than the diploids, but Distribution. Japan (Kanto region and East it does not grow in alpine regions. Shizuoka pref.). Japanese name. Nankai-miyama-katabami. Habitat. Oxalis nipponica var. kantoensis oc- Representative specimens examined. Japan. Tosa: curs at relatively lower elevations (sea level to ca. Tsuetate toge, 26 July 1888, collector unknown s.n. (TI). 500 m) in shady, wet environments, such as river- Kumamoto: Kuma, Gokimura, April 1908, collector un- sides, valley lines and on the north-facing slopes known s.n. (TI). Tosa: Agawa village, S. Watanabe s.n. of mountains. (MAK72624). Kochi: Agawa village, T. Makino s.n. (MAK72626). Mt. Takao, T. Makino s.n. (MAK72597). Mt. Takao, T. Makino s.n. (MAK72590). Japanese name. Kantou-miyama-katabami.
Representative specimens examined. Japan. Sagami: Oyama, 17 May 1900, collector unknown s.n. (TI). Mt. 6. Oxalis trilliifolia Hook., Fl. Bor.-Amer. 118. Tsukuba, T. Makino s.n. (MAK72596). Mt. Takao, T. 1831. as "trilliifolium" Makino s.n. (MAK72598 three sheets). Mt. Takao, April ≡ Hesperoxalis trilliifolia (Hook.) Small, N. 1904, T. Makino s.n. (MAK72599). Mt. Tsukuba, collec- Amer. Fl. 25: 27. 1907. – Type: USA. near Great tor unknown s.n. (MAK72595). Hakone, collector un- Rapids of Columbia River, Douglas s.n. (holo- K known s.n. (MAK72601). Mt. Tsukuba, O. Suzuki s.n. (MAK72717). 000693111 digital image!).
Rhizomes covered with bases of petioles. Leaf- 5b-II. var. alpigena S. Aoki & J. Murata, lets obcordate. Flowers umbellate, 3–12 florets var. nov. ––Fig. 3. per inflorescence; petals white. Capsules oblong.
Oxalis nipponica var. alpigena has been confused with O. acetosella. It can be distinguished from O. acetosella by Distribution. Western North America. its obtriangular leaves, and from O. nipponica var. kan- Digitized specimens examined. USA. Washington: toensis by the smaller capsules and seeds. Clark Country, Whipple Creek County, 11 September Typus. Japan, Kagoshima: Mt. Shibi, 20 June 2015, S. 2015, Park Ben Legler 13860 (WTU). Washington: Pierce Aoki 239 (holo- TI!). County, 15 May 2014, Etsuko Reistroffer 31 (WTU). Or- [Oxalis acetosella L. var. acetosella sensu egon: Lincoln County, Coast Range, Gwynn Creek, 31 Terao in Acta Phytotax. Geobot. 30: 58. 1979, pro August 2007, Mark Fishbein 6042 (HPSU). All speci- mens were observed at the Consortium of Pacific North- parte excl. typ.] west Herbaria Specimen Database (CPNWH).
Rhizomes often elongate. Longest vein of termi- nal leaflet ca. 9–17 mm long; Petals always with 7. Oxalis montana Raf. in Amer. Monthly Mag. October 2019 Aoki & al. – Taxonomic Revision of subsect. Oxalis 169
Fig.2. Oxalis nipponica subsp. nipponica. A: Habit. B: Leaf. C: Rhizome. D: Flower, front view. E: Flower, side view. F: Fruit. (A–E: Japan, Tottori Pref., Mt. Nagi, 23 April 2018. F: Japan, Yamaguchi Pref., Souzu-kyo, 22 April 2018.).
Fig.3. Oxalis nipponica subsp. kantoensis var. alpigena. A: Habit. B: Leaf. C: Rhizome. D: Flower, front view. E: Flower, side view. F: Fruit. (A–E: Japan, Miyazaki Pref., Mt. Wanitsuka, 10 April 2018. F: In cultivation, originally collected on Mt. Wanitsuka on 4 July 2018.). 170 Acta Phytotax. Geobot. Vol. 70
& Crit. Rev. 2: 266. 1818. Peck in Leafl. W. Bot. 7: 185–186. 1954. ≡ Oxalis ≡ O. acetosella L. subsp. montana (Raf.) Hul- oregana f. smalliana (R. Knuth) Munz in Aliso 4: tén in Kongl. Svenska Vetensk. Acad. Handl., n.s. 93. 1958. – Type: USA, California: Monterey Co., 7:146. 1958. – Type: Not designated. Santa Lucia Mountains, R. A. Plaskett 25 (holo- = O. americana Bigelow ex DC., Prodr. 1: NY 00373733 digital image!). 700. 1824. – Type: Amer. bor. umbrosis, J. Big- elow (lecto- G-DC 217757/1 digital image! desig- Rhizomes covered with bases of petioles. Leaf- nated by Lourteig 2000, International Code of lets obcordate. Flowers solitary; petals white or Nomenclature Art. 9.9 (Turland et al. 2018)). pink, sometimes with pink veins. Capsules glob- = O. americana Bigelow ex DC. f. rhodantha ular. Fernald in Rhodora 20: 78. 1918. ≡ O. montana Raf. f. rhodantha (Fernald) Fernald in Rhodora Distribution. Western coastal North America. 22: 144. 1920. ≡ O. acetosella L. var. rhodantha (Fernald) R. Knuth, Pflanzenr. 438. 1930. ≡ O. Notes. Oxalis oregana var. tracyi Jeps., Man. acetosella L. var. acetosella f. rhodantha (Fer- Fl. Pl. Calif. 588. 1925. needs further research to nald) Geerinck & Walravens in Taxonomania 20: determine its taxonomic status. 1–4. 2007. – Type: USA, New Hampshire, C. E. Possible syntypes of O. oregana are listed as Faxon s.n. (holo- GH 00043712 digital image!). follows: USA, Oregon, T. Nuttall s.n. (GH 00100450 digital image!); USA, Oregon, T. Nut- Rhizomes elongate, covered with scale leaves tall s.n. (NY 373734 digital image!). and bases of petioles. Scale-like leaves triangular, sericeous when young. Base of petioles scaly, tri- Digitized specimens examined. USA. California: angular, sericeous when young, abscission layer Humboldt County, Trinidad Sate Beach, 18 August 2010, round. Leaflets obcordate, ciliate; both surfaces C. Davidson 11787 (SRP). California: Humboldt County, Blair Grove, 18 May 1992, Michael R. Hays 491 (ID). pubescent. Flowers solitary; petals white or pink. California: Del Norte County, 6 May 1967, Gary Kuhl s.n. Capsules globular. Seeds brown, asymmetrically (SOC). All specimens were observed at CPNWH. ovoid, longitudinally ridged.
Distribution. Eastern North America. Oxalis acetosella L. × O. nipponica S. Aoki & Specimens examined. Canada. Newfoundland: Burnt Islands, 1989, A. Bouchard et al. 89216 (GH). USA. Vir- J. Murata subsp. nipponica ginia: Pembroke, 13 July 2015, S. Aoki 416 (TI). ≡ O. acetosella L. subsp. acetosella var. ace- tosella × O. acetosella L. subsp. griffithii(Edgew. & Hook.f.) H. Hara var. griffithii Terao in Acta 8. Oxalis oregana Nutt. ex Torr. & A. Gray, Fl. Phytotax. Geobot. 30: 62. 1979. – Type: Japan, N. Amer. 1: 211. 1838. Nagano: Kamikochi, 21 May 1978, H. Terao 250 ≡ Oxalis acetosella L. var. oregana (Torr. & (holo- KYO!). A. Gray) Trel. in Mem. Boston Soc. Nat. Hist. 4: 90. 1888. ≡ Oxalis acetosella L. subsp. oregana Morphologically similar to O. nipponica. Base of petals with yellow spots. Leaflets obtriangular with slightly (Torr. & A. Gray) D. Löve in Taxon 17: 89. 1968. round corner. Chasmogamous and cleistogamous flowers – Type: USA. Oregon, woods, T. Nuttall s.n.; J. present. Capsules not seen. Genome size is approximately Scouler s.n. intermediate between the parental taxa. = O. smalliana R. Knuth, nom. nov. in Notiz- bl. Bot. Gart. Berlin-Dahlem. 308. 1919, based on Distribution. Japan, Nagano Pref., Kamiko- O. macra Small, N. Amer. Fl. 25(1): 26. 1907, not chi, on level ground preferred by O. nipponica O. macra Schltr., Bot. Jahrb. Syst. 27: 155. 1900. rather than O. acetosella. ≡ O. oregana var. smalliana (R. Knuth) M. Ecology. Oxalis acetosella L. × O. nipponica October 2019 Aoki & al. – Taxonomic Revision of subsect. Oxalis 171 subsp. nipponica coexists with the parental taxa, C.-F., T.-C. Huang, Z.-Y. Li, H.-C. Lo, H. Ohashi, but is rare. The parental taxa at this site flower at C.-F. Shen, J.-C. Wang & K.-C. Yang (eds.), Flora of Taiwan, 2nd ed., vol. 3. second edition, pp. 397–402. the same time. The hybrid appears to occur at low The editorial committee of the Flora of Taiwan, Tai- frequency in this populations. Oxalis nipponica pei. at the same site lacks spots on the petals. Knuth, R. G. P. 1914. Ein Beitrag zur Systematik und geographischen Verbreitung der Oxalidaceen. Bot. Notes. A sample of Oxalis acetosella L. × O. Jahrb. Syst. 50 (supple.): 215–237 (in Germany). Knuth, R. G. P. 1930. Das Pflanzenreich 95. Verlag von nipponica subsp. nipponica from this locality had Wilhelm Engelmann, Leipzig. the ITS type of O. nipponica subsp. nipponica Linnaean herbarium – the Linnaean Collections. 2018. and the chloroplast haplotype of O. acetosella
Tzvelev, N. N. 1988. Oxalidaceae. In: Kharkevich, S. S. Yonekura, K. 2011. Taxonomic notes on vascular plants in (ed.) ,Plantae vasculares orientis extremi sovietici 3. Japan and its adjacent regions (II). J. Jap. Bot. 86: pp.136–139. Nauka, Leningrad (in Russian). 230–241.
Received September 13, 2018; accepted April 1, 2019