J. Jpn. Bot. 92(2): 119–122 (2017)

a, b Kenji Suetsugu * and Takuto Shirata : A New Color Variant of the Slipper Orchid debile aDepartment of Biology, Graduate School of Science, Kobe University, 1-1, Rokkodai, Nada-ku, Kobe, 657-8501 JAPAN; bGraduate School of Life and Environmental Sciences, Tsukuba University, 1-1-1, Tennodai, Tsukuba, 305-8571 JAPAN *Corresponding author: [email protected]

Summary: We describe a new form of and locally common species found in , Cypripedium debile whose lip excepting basal Taiwan, and Japan (Cribb 1997). It can be area, column, stigma, and staminode is lacking in distinguished from other species in its genus by purple coloration in Kiso County, Nagano Pref., its glabrous habit, its paired heart-shaped leaves Japan The ecological significance of the new that are borne well above the soil surface, and its form Cypripedium debile f. shinanoense is also discussed. pendent inflorescence that bear small green and dark purple-veined flowers that are subtended The lady’s slippers subfamily by a linear bract (Cribb 1997). The current study (), which is distributed describes a new form of C. debile that has lips throughout the northern temperate zone and lacking the dark purple veins. some of the tropics, is often regarded as a model lineage for food-deceptive orchids. Taxonomic treatment The Cypripedioideae contains five genera Cypripedium debile Rchb. f. f. shinanoense comprising a total of 158 species (Pridgeon et al. Suetsugu & Shitara, f. nov. [Fig. 1] 2001). One of the distinguishing features of this The newly discovered specimens differ from group is the one-way trap design of their flowers, Cypripedium debile Rchb. f. f. debile in that the which facilitates efficient pollination. Visiting lip excepting basal area, column, stigma, and insects pass through the flower entrance into the staminode is lacking in purple coloration. labellum and then proceed to exit through one of Type: JAPAN. Honshu. Nagano Pref., the pairs of basal orifices that are formed by the Kiso County, Agematsu Town. 4 June 2016, staminode that block the opening at the bottom Masayuki Matsui 160604-1 (KPM–holotype). of the labellum (Li et al. 2008). Japanese name: Shinano-ko-Atsumorisō. The genus Cypripedium is a group of lady’s Note: In this habitat, approximately 200 slippers orchids that contains ca. 50 species flowering individuals ofC. debile f. shinanoense found throughout northern temperate zones were found growing on the floor of the (Cribb 1997, Pridgeon et al. 2001). Although coniferous forest dominated by Chamaecyparis species belonging to this genus are generally obtusa (Siebold et Zucc.) Endl. and Abies firma considered to be bee pollinated (Sugiura et Siebold et Zucc. None of C. debile f. debile al. 2001, Sugiura et al. 2002, Bänziger et al. are distributed in the habitat. Similar color 2005, Suetsugu and Fukushima 2014, but also variants have also been discovered, though see Ren et al. 2011), it has been suggested the mutant has not been formally described that one species, Cypripedium debile Rchb. f., with a type specimen (Mitsuhashi 1988). In might utilize its mushroom-like odour to attract addition, a previously recognized mutant is fungivorous flies (Stoutamire 1967). somewhat distinct from C. debile f. shinanoense Cypripedium debile Rchb. f. is a widespread because the flower of the previously recognized

—119— 120 植物研究雑誌 第 92 巻 第 2 号 2017 年 4 月 Suetsugu & Shitara from the type locality. K. Flower. L. Flower without without Flower L. Flower. K. locality. type the from Shitara & Suetsugu shinanoense f. f. C. debile debile C. from Minami-tsuru-gun, Yamanashi Pref. A. Flower. B. Flower without dorsal sepal. C. Lip. D. Dorsal sepal. E. Lateral Lateral E. sepal. Dorsal D. Lip. C. sepal. dorsal without Flower B. Flower. A. Pref. Yamanashi Minami-tsuru-gun, from debile Rchb. f. f. f. Rchb. Cypripedium debile debile Cypripedium dorsal sepal. M. Lip. N. Dorsal sepal. O. Lateral sepal. P. Lateral petal. Q. Longitudinal section of lip. R, S. Column. Bar = 3mm. 3mm. = Bar Column. S. R, lip. of section Longitudinal Q. petal. Lateral P. sepal. Lateral O. sepal. Dorsal N. Lip. M. sepal. dorsal sepal. F. Lateral petal. G. Longitudinal section of lip. H, I. Column. K–S. K–S. Column. I. H, lip. of section Longitudinal G. petal. Lateral F. sepal. Fig. 1. A–I. 1. A–I. Fig. April 2017 The Journal of Japanese Botany Vol. 92 No. 2 121 color variant is completely lacking in purple Hashiba, Michiko Mineta, and Sadayoshi coloration including the basal area of the lip and Mineta for their assistance in the field study. We lateral petal, which is still purple in C. debile f. also thank Masayuki Sato for providing typical shinanoense (Mitsuhashi 1988). In addition, as C. debile f. debile samples to utilize in the far as we know, a color variant of C. debile that comparative study. This work was supported by is completely lacking purple coloration in the JSPS KAKENHI Grant Number 15K18470. flower often co-occurs at very low frequency with normal colored C. debile populations, References while as many as 200 C. debile f. shinanoense Bänziger H., Sun H. and Luo Y. B. 2005. Pollination of flowering individuals occur without C. debile f. a slippery lady slipper orchid in south-west China: debile. These facts may indicate that C. debile Cypripedium guttatum (). Bot. J. Linn. Soc. 148: 251–264. f. shinanoense is ecologically distinct from the Cribb P. 1997. The Genus Cypripedium. Timber Press, color variant of C. debile, which is completely Portland. lacking purple coloration in the flower. It should Li P., Luo Y. B., Deng Y. X. and Kou Y. 2008. Pollination be noted that Mitsuhashi (1988) also noted that of the lady’s slipper Cypripedium henryi Rolfe (Orchidaceae). Bot. J. Linn. Soc. 156: 491–499. the color variant of C. debile that is completely Mitsuhashi S. 1988. Mezurashii-yaseiran [Rare Wild lacking purple coloration in flower can be seen Orchid]. Ikeda Publishing Co. Ltd., Tokyo (in without C. debile f. debile in a population. Japanese). However, unfortunately, the population Policha T., Davis A., Barnadas M., Dentinger B., Raguso Mitsuhashi (1988) indicated has been lost R. A. and Roy B. A. 2016. Disentangling visual and olfactory signals in mushroom mimicking Dracula due to illegal collection (Mitsuhashi personal orchids using realistic three-dimensional printed communication). flowers. New Phytol.210 : 1058–1071. Cypripedium debile Rchb. f., is believed Pridgeon A. M., Cribb P. J., Chase M. W. and Rasmussen to utilize its mushroom-like odour to attract F. N. 2001. Genera Orchidacearum. Vol. 1. Oxford University Press, New York. fungivorous flies (Stoutamire 1967). In addition Roy B. A. and Raguso R. A. 1997. Olfactory versus visual to their mushroom-like odour, the dark purple cues in a floral mimicry system. Oecologia 109: 414– veins on the lips of C. debile flowers bear a 426. striking resemblance to the gills of mushrooms, Ren Z. X., Li D. Z., Bernhardt P. and Wang H. 2011. which suggest that this species utilizes not only Flowers of Cypripedium fargesii (Orchidaceae) fool flat-footed flies (Platypezidae) by faking fungus- olfactory mimicry to attract pollinators but also infected foliage. Proc. Natl. Acad. Sci. USA. 108: visual signals. Indeed, Policha et al. (2016) has 7478–7480. shown that the mushroom-like, ‘gilled’ labellum Stoutamire W. 1967. Flower biology of the Lady’s Slipper of the orchid Dracula lafleurii can enhance (Orchidaceae: Cypripedium). Michigan Botanist 6: 159–175. pollinator attraction by exploiting the visual/ Suetsugu K. and Fukushima S. 2014. Pollination biology chemosensory perceptual bias of fungivorous of the endangered orchid Cypripedium japonicum in drosophilid flies. Given the apparent importance a fragmented forest of Japan. Spec. Biol. 29: of this phenomenon, it would be interesting to 294–299. investigate whether the absence of the purple Sugiura N., Fujie T., Inoue K. and Kitamura K. 2001. Flowering phenology, pollination, and fruit set of veins on the lips of the newly discovered form Cypripedium macranthos var. rebunense, a threatened of C. debile affects the frequency of pollinator lady’s slipper (Orchidaceae). J. Plant Res. 114: 171– visits or the diversity of its pollinator assemblage 178. in comparison to C. debile f. debile. Sugiura N., Goubara M., Kitamura K. and Inoue K. 2002. Bumblebee pollination of Cypripedium macranthos var. rebunense (Orchidaceae); a possible case of floral We thank Masayuki Matsui for his discovery. mimicry of Pedicularis schistostegia (Orobanchaceae). We also thank Masayuki Matsui, Kenichi Plant Syst. Evol. 235: 189–195. 122 植物研究雑誌 第 92 巻 第 2 号 2017 年 4 月

a b 末次健司 ，設楽拓人 ：ラン科コアツモリソウの色彩 変異 コ ア ツ モ リ ソ ウ Cypripedium debile Rchb. f.（ ラ ン ツモリソウは，キノコに似た匂いとキノコのヒダに似た 科）の唇弁には，通常，顕著な暗紫色の脈を生じるが， 唇弁の脈により，菌食性の昆虫を送粉者として利用して この脈を生じない個体が新たに見つかったので，新品 いると考えられている．よって，脈を生じない新品種に 種シナノコアツモリソウ Cypripedium debile Rchb. f. f. おいて，母種と送粉様式に違いがあるかは興味のあると shinanoense Suetsugu & Shitara として記載した．タイプ ころである． 産地では，およそ 200 個体すべてが暗紫色の脈を生じ （a神戸大学理学研究科， ない個体で，通常の個体とは混生していなかった．コア b筑波大学生命環境科学研究科）