ISSN 1346-7565 Acta Phytotax. Geobot. 69 (1): 69–74 (2018) doi: 10.18942/apg.201717 Short Communication First Record of the Mycoheterotrophic Sciaphila corniculata () from Ishigaki Island, Ryukyu Islands, Japan, with Updated Description of its Morphology, in particular on Stylar Characteristics

1,* 2 Kenji Suetsugu and Takaomi Sugimoto

1Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe, 657-8501, Japan. *[email protected] (author for correspondence); 2Entomological Laboratory, Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Hakozaki 6-10-1, Higashi-ku, Fukuoka 812-8581, Japan

We report three new localities of the mycoheterotrophic plant Sciaphila corniculata (Triuridaceae) from Ishigaki Island, Ryukyu Islands, Japan. Previously, S. corniculata was reported only from Kolombang- ara Island (Solomon Islands), Waigeo Island (New Guinea) and Obi and Aru islands (the Moluccas). We also update a description of its morphology, in particular on stylar characteristics based on new materi- als. A key to the Japanese species of Sciaphila based on total flower and stylar characteristics is also pro- vided for easy identification of these rare mycoheterotrophic .

Key words: Distribution, mycoheterotrophy, Sciaphila, , Triuridaceae

The Triuridaceae comprise fully mycohetero- small, up to 40 cm tall, recognizable only during trophic plants that mainly grow in deep shade un- the reproductive season and usually occur in derstory in ever-wet forests in the tropics and small populations. Consequently, they have subtropics worldwide, reaching their northern- scarcely been collected and their morphological most limits in temperate regions of Japan (van de traits rarely described in detail. In addition, key Meerendonk 1984). The mycoheterotrophic characteristics of the staminate flowers, which Sciaphila Blume consists of ca. 40 species and is are crucial for precise identification, have not the largest genus in the family (van de Meeren- been documented in some species, particularly in donk 1984). individuals too young at the time of collection or In taxonomic studies of Sciaphila (van de because staminate flowers are often limited (Tsu- Meerendonk 1984, Hsieh et al. 2003, Chanta- kaya & Okada 2013, Tsukaya & Suetsugu 2014). naorrapint & Thaithong 2004, Averyanov 2007, Given the difficulty of precise identification, the Ohashi et al. 2008, Xu et al. 2011, Tsukaya & taxonomy of Sciaphila remains to be revised. Okada 2013, Tsukaya & Suetsugu 2014, Suetsugu Japan is known for its great diversity of et al. 2016a, Suetsugu & Nishioka 2017), the fol- Sciaphila, harboring seven species (Suetsugu et lowing floral traits have been used as key charac- al. 2016a, Suetsugu & Nishioka 2017). In fact, the ters for species discrimination: bisexual or uni- flora of Japan is particularly rich in mycohetero- sexual flowers, number and shape of the stamens trophic plants, harboring ca. 50 species. Recent and perianth segments, shape of the apical peri- botanical surveys of mycoheterotrophic plants in anth segments, and shape and length of the styles. Japan have resulted in the discovery of several As with most mycoheterotrophs, the plants are new distributional records and new taxa (Ohashi 70 Acta Phytotax. Geobot. Vol. 69

Fig. 1. Habit and microscopic images of Sciaphila corniculata on Ishigaki Island. A. . B. Carpellate flower. C. Staminate flower. Bar = 0.2 mm (B), 0.1 mm (C). et al. 2008, Yagame et al. 2008, Yahara & Tsu- pan. We also provide a description based on the kaya 2008, Suetsugu 2012a, b, 2013, 2014, 2015a, plants from Ishigaki Island, because there are a b, 2016a, b, c, d, 2017, Suetsugu & Ishida 2011, few minor differences between previous descrip- Suetsugu et al. 2012, 2013, 2014b, 2016a, b, Su- tions and the plants on Ishigaki Island. etsugu & Yagame 2014, Suetsugu & Fukunaga 2016). Of particular interest are the lowland for- Sciaphila corniculata Becc., Malesia 3: 336. (1890) ests of the Ryukyu Islands, which are known to — Figs. 1–2. be a hotspot for endemic mycoheterotrophic taxa such a Sciaphila yakushimensis Suetsugu, Tsuka- Specimen examined: JAPAN. Ryukyu. Okinawa Pref., Ishigaki City, Nosoko, alt ca. 10 m, 18 October ya & H. Ohashihashi, Gastrodia takeshimensis 2015, T. Sugimoto s.n. (KYO); JAPAN. Ryukyu. Okinawa Suetsugu and Gastrodia flexistyloides Suetsugu. Pref., Ishigaki City, Nosoko, alt ca. 20 m, 15 October A detailed botanical survey of the Ryukyu Is- 2016, T. Sugimoto s.n. (KYO); JAPAN. Okinawa Pref., lands would likely provide more precise data re- Ishigaki City, Miyara, alt. ca. 80 m, 21 October 2016, T. garding the diversity and distribution of myco- Sugimoto s.n. (OSA); JAPAN. Okinawa Pref., Ishigaki City, Nosoko, alt ca. 10 m, 30 September 2016, T. Nishio- heterotrophs. As anticipated, during a recent bo- ka s.n. (OSA); JAPAN. Okinawa Pref., Ishigaki City, tanical survey, we collected unknown plants of Ibaruma, alt ca. 170 m, 30 September 2016, T. Nishioka Sciaphila in lowland evergreen forests on Ishiga- s.n. (OSA). ki Island, Ryukyu Islands. After a detailed mor- phological investigation, we determined them to Herbs, monoecious, mycoheterotrophic, pe- be Sciaphila corniculata Becc. (Fig. l). Here we rennial, erect, carmine or scarlet, non-branched; report the first occurrence of that species in Ja- underground parts white. Roots filiform, with February 2018 Suet sugu & Sugimoto — Sciaphila corniculata, new to Japan. 71

Fig. 2. Sciaphila corniculata on Ishigaki Island A. Flowering plant, B. Staminate flower, C. Carpellate flower. D. Carpellate flower in fruit with persistent perianth segments. E. Anthers with floral disc. F. Immature carpel with stigma. G. Immature fruit. Bar = 5 mm (A), 0.5 mm (B–G). Drawn by Kumi Hamasaki. few hairs. Inflorescences glabrous, 1.5–6 cm tall, ers distal. Pedicels ca. 0.7–1.5 mm long, straight, ca. 0.8 mm thick. Scale leaves acute, ca. 1.5 mm shorter than flower, divergent at 60–90°; bracts long. Inflorescences racemose, rachis ca. 0.5–2 linear, acute, ca. 1 mm long, appressed to the cm long, densely 3–11 flowered, staminate flow- pedicel. Staminate flowers 1.6–1.8 mm across, 72 Acta Phytotax. Geobot. Vol. 69 perianth segments 6, opening flat, equal in size, Island (New Guinea; H. Tsukaya, personal com- connate at base, segments ovate to triangular, munication). We consider the differences to most glabrous, apex acute, long-bearded. Stamens 3, likely represent intraspecific variation, mainly without filaments. Anthers 4-lobed. Carpellate due to floral conditions. flowers: 1.8–2.1 mm across; perianth segments 6, equal in size, connate at base, segments ovate to Distribution and phenology. Sciaphila cor- triangular, glabrous, apex obtuse or acute, with- niculata has been reported only from Kolomban- out particular structures. Carpels numerous, el- gara Island (Solomon Islands), Waigeo Island lipsoidal, ca. 0.2–0.3 mm long, apex rounded; (New Guinea) and Obi and Aru islands (the Mo- style and stigma clavate with dense cylindrical luccas); the Japanese populations represent the papillae or rarely subulate with inconspicuous cy- northernmost occurrence of the species. lindrical papillae, laterally inserted at base of The S. corniculata populations in Japan ap- ovary; free portion of style and stigma ca. 0.6–0.7 pear to be restricted to three locations separated mm long. by at least 1 kilometers on central Ishigaki Island, Ryukyu Islands, Japan. They occur at approxi- Taxonomic note. The staminate flowers of mately 10–170 m elevation within a humid ever- Sciaphila on Ishigaki Island bear unisexual flow- green broadleaved forest dominated by Cas- ers with six equal-sized perianth segments, indi- tanopsis sieboldii (Makino) Hatus. ex T. Yamaz. cating that they belong to Sciaphila sect. Oligan- & Mashiba, Distylium racemosum Siebold et thera subsect. Quadrilobatae (van de Meeren- Zucc, and Neolitsea aciculata (Blume) Koidz. donk 1984). Subsection Quadrilobatae contains Sciaphila corniculata flowers from mid-Septem- several species, including S. corniculata Beccari, ber to mid-October. Each location consisted of S. secundiflora Thwaites ex Bentham, S. stellata dozens of individuals, together totaling less than Aver., S. thaidanica K. Larsen and S. alba Tsu- 50 flowering plants. We are not aware of any oth- kaya and Suetsugu. However, our material differs er localities for S. corniculata on Ishigaki Island. from S. secundiflora, S. stellata, S. thaidanica Given that mycoheterotrophic plants are high- and S. alba in having a long beard at the apex of ly dependent on the activities of both the fungi all 6 staminate perianth segments. The character- and the trees that sustain them (e.g., Suetsugu et istics of the plants on Ishigaki Island closely al. 2014a), they are particularly sensitive to envi- match the description of S. corniculata (van de ronmental destruction. Careful conservation is Meerendonk 1984). Based on morphological sim- requested for these populations. It should also be ilarities of the other floral organs, we determined noted that S. corniculata may be found more our material to be S. corniculata. widely, considering that these mycoheterotrophic Despite the similarities, there are a few minor plants are easily overlooked. Further exploration differences between the plants on Ishigaki Island is needed to elucidate the full distribution of S. and previous descriptions and illustrations of S. corniculata in Japan. corniculata. For example, S. corniculata was of- ten described as having a subulate style, with a glabrous apex (Schlechter 1912, van de Meeren- We are grateful to Mrs. Tatsuki Nishioka and Ryosuke donk 1984). In contrast, plants in the Ishigaki Uchiyama for assistance in the field study. The beautiful, very helpful line drawings were prepared by Ms. Kumi population always have a clavate style with dense, Hamasaki. We are also grateful to Dr. Hirokazu Tsukaya cylindrical papillae (Fig. 1A). Our observations for useful discussions on the taxonomic treatments. This of the Ishigaki plants revealed that the style tends work was financially supported by the Toyota Foundation to shrink from the apex during the late flowering and the JSPS KAKENHI (17H05016 to KS). stage and appears to be subulate (Fig. 1B). Cla- vate styles with dense cylindrical papillae were noticed in some plant of S. corniculata on Waigeo February 2018 Suet sugu & Sugimoto — Sciaphila corniculata, new to Japan. 73

A. Key to the Species of Sciaphila in Japan based on general floral characteristics (modified after Suetsugu & Nishioka 2017)

1a. Plants with bisexual and unisexual flowers ...... S. tenella 1b. Plants with unisexual flowers ...... 2 2a. Staminate flowers located between carpellate flowers ...... S. multiflora 2b. Staminate flowers located above carpellate flowers...... 3 3a. Segments of staminate flower equal ...... 4 3b. Segments of staminate flowers unequal, 3 large alternating with 3 small ...... 5 4a. Staminate flowers ca. 6–7 mm across ...... S. secundiflora 4b. Staminate flowers ca. 1.5–2.0 mm across ...... 6 5a. Apex of all 6 staminate perianth segments with globose knob ...... S. sugimotoi 5b. Apex of only 3 smaller staminate perianth segments with globose knob ...... 7 6a. Staminate perianth segments without beard ...... S. ramosa 6b. Staminate perianth segments with apical beard ...... S. corniculata 7a. Style subulate, apex smooth, glabrous ...... S. nana 7b. Style club-shaped, papillate ...... S. yakushimensis

B. Key to the Species of Sciaphila in Japan based primarily on stylar characteristics (modified after Suetsugu & Nishioka 2017)

1a. Style of carpellate flowers club-shaped, apex papillate ...... 2 1b. Style of carpellate flowers subulate, apex glabrous...... 6 2a. Flowers staminate and bisexual; apex of perianth bearded ...... S. tenella 2b. Flowers unisexual ...... 3 3a. Staminate flowers located between carpellate flowers ...... S. multiflora 3b. Staminate flowers above carpellate lowers...... 4 4a. Staminate flowers 6–7 mm across; carpellate flowers ca. 5 mm across; perianth segments of staminate flowers narrowly triangular to linear-triangular, equal, apex without appendage; plants reddish purple or brownish pink ..... S. secundiflora 4b. Staminate and carpellate flowers of same size, less than 2.5 mm across; perianth segments of staminate flowers narrowly ovate to triangular ...... 5 5a. Staminate flowers, ca. 1.5 mm across; perianth segments dimorphic, 3 broader alternating with 3 narrower; apx of narrower segments with globose knob; plants blackish purple ...... S. yakushimensis 5b. Staminate perianth segments, ca. 2 mm across, equal in size; apex of all segments bearded; plants carmine to scarlet ...... S. corniculata 6a. Perianth segments monomorphic; apex of perianth without appendages ...... S. ramosa 6b. Perianth segments dimorphic, 3 broader alternating with 3 narrower; apex of perianth segments with globose knob ...... 7 7a. Connective exceeding anthers; apex of 3 narrower staminate perianth segments with globose knob ...... S. nana 7b. Connective not exceeding anthers; apex of all staminate perianth segments with globose knob ...... S. sugimotoi

239–247. References van de Meerendonk, J. P. M. 1984. Triuridaceae. In: Stee- nis, C. G. G. J. van (ed.) Flora malesiana ser. I, 10, pp. Averyanov, L. V. 2007. The genus Sciaphila Blume (Tri- 109–121. Martinus Nijhoff, The Hague, Boston, Lon- uridaceae) in the flora of Vietnam. Taiwania 52: 12– don. 19. Ohashi, H., H. Kato, S. Kobayashi, & J. Murata. 2008. A Chantanaorrapint, S. & O. Thaithong. 2004. Sciaphila revision of Triuridaceae of Japan. J. Jpn. Bot. 83: 20– nana Blume (Triuridaceae), a new record for Thai- 35. land. Thai Forest Bulletin (Botany) 32: 12–14. Schlechter, R. 1912. Neue Triuridaceae Papuasiens. Bot. Hsieh, T. H., C. S. Wu & K. C. Yang. 2003. Revision of Jahrb. Syst. 49: 70–89. Sciaphila (Triuridaceae) in Taiwan. Taiwania 48: Suetsugu, K. 2012a. A new form of Gastrodia confusa 74 Acta Phytotax. Geobot. Vol. 69

(Orchidaceae). J. Phytogeogr. Taxon. 59: 125–126. Suetsugu, K. & T. Yagame. 2014. Color variation of the Suetsugu, K. 2012b. New record of the mycoheterotro- mycoheterotrophic orchid Yoania japonica. Acta phic orchid Lecanorchis kiusiana forma lutea outside Phytotax. Geobot. 65: 45–47. the type locality. J. Phytogeogr. Taxon. 60: 35–37. Suetsugu, K., M. Nakama, T. Watanabe, H. Watanabe & Suetsugu, K. 2013. Gastrodia takesimensis (Orchidace- M. Yokota. 2012. The northernmost locality of Gas- ae), A new mycoheterotrophic species from Japan. trodia shimizuana (Orchidaceae). J. Jpn. Bot. 87: 62– Ann. Bot. Fennici 50: 375–378. 64. Suetsugu, K. 2014. Gastrodia flexistyloides (Orchidace- Suetsugu, K., M. Nakayama, T. Watanabe, H. Watanabe, ae), a new mycoheterotrophic plant with complete T. Yamamoto & M. Yokota. 2013. First record of the cleistogamy from Japan. Phytotaxa 175: 270–274. mycoheterotrophic plant Gastrodia clausa (Orchida- Suetsugu, K. 2015a. The mysterious life of plants that ceae) from Okinawa Island, Ryukyu Islands, Japan. have lost their photosynthetic ability and eat fungi. Acta phytotax. Geobot. 64: 123–126. Bunrui 15: 99–108. (in Japanease). Suetsugu, K., A. Kawakita & M. Kato. 2014a. Evidence Suetsugu, K. 2015b. First record of the mycoheterotro- for specificity to Glomus group Ab in two Asian my- phic orchid Gastrodia uraiensis (Orchidaceae) from coheterotrophic Burmannia species. Pl. Spec. Biol. Yakushima Island, Japan. Acta Phytotax. Geobot. 66: 29: 57–64. 193–196. Suetsugu, K., H. Umata & M. Yokota. 2014b. First record Suetsugu, K. 2016a. A new color variant of the mycohet- of the mycoheterotrophic orchid Gastrodia fontinalis erotrophic orchid Gastrodia fontinalis from Takeshi- (Orchidaceae) from Takeshima Island, the Ryukyu ma Island, Japan. Acta Phytotax. Geobot. 67: 55–59. Islands, Japan. Taiwania 59: 383–386. Suetsugu, K. 2016b. A new color variant of the mycohet- Suetsugu, K., T. C. Hsu, H. Fukunaga & S. Sawa. 2016a. erotrophic orchid Cyrtosia septentrionalis from Hi- Epitypification, emendation and synonymy of roshima Prefecture, Japan. J. Jpn. Bot. 91: 250–253. Lecanorchis taiwaniana (Vanilleae, Vanilloideae, Suetsugu, K. 2016c. New locality of the mycoheterotro- Orchidaceae). Phytotaxa 265: 157–163. phic orchid Gastrodia fontinalis from Kuroshima Is- Suetsugu, K., H. Tsukaya & H. Ohashi. 2016b. Sciaphila land, Kagoshima Prefecture, Japan. J. Jpn. Bot. 91: yakushimensis (Triuridaceae), a new mycoheterotro- 358–361. phic plant from Yakushima Island, Japan. J. Jpn. Bot. Suetsugu, K. 2016d. Gastrodia kuroshimensis (Orchida- 91: 1–6. ceae: Epidendroideae: Gastrodieae), a new mycohet- Tsukaya, H. & H, Okada. 2013. Two new species of erotrophic and complete cleistogamous plant from Ja- Sciaphila Blume (Triuridaceae) from Kalimantan, pan. Phytotaxa 278: 265–272. Borneo, with a new record of S. thaidanica from Bor- Suetsugu, K. 2017. Two new species of Gastrodia (Gas- neo. Syst. Bot. 38: 600–605. trodieae, Epidendroideae, Orchidaceae) from Okina- Tsukaya, H. & K, Suetsugu. 2014. Two new species of wa Island, Ryukyu Islands, Japan. Phytotaxa 302: Sciaphila (Triuridaceae) from Sarawak (Borneo, Ma- 251–258. laysia). Phytotaxa 170: 283–290. Suetsugu, K. & K. Ishida. 2011. New locality and fungal Xu, H., Y. D. Li & H. Q. Chen. 2011. A new species of association of Thismia abei (Thismiaceae). J. Phyto- Sciaphila (Triuridaceae) from Hainan Island, . geogr. Taxon. 59: 43–45. Novon 21: 154–157. Suetsugu, K. & H. Fukunaga. 2016. Lecanorchis tabuga- Yagame, T., T. Katsuyama & T. Yukawa. 2008. A new waensis (Orchidaceae, Vanilloideae), a new mycohet- species of Neottia (Orchidaceae) from the Tanzawa erotrophic plant from Yakushima Island, Japan. Phy- Mountains, Japan. Acta Phytotaxonomica et Geobo- tokeys 73: 125–135. tanica 59: 219–222. Suetsugu, K. & T. Nishioka. 2017. Sciaphila sugimotoi Yahara, T. & H. Tsukaya. 2008. Oxygyne yamashitae, a (Triuridaceae), a new mycoheterotrophic plant from new species of Thismiaceae from Yaku Island, Japan. Ishigaki Island, Japan. Phytotaxa. 314: 279–284. Acta Phytotax. Geobot. 59: 97–104.

Received March 21, 2017; accepted August 25, 2017