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Kobe University Repository : Kernel Time-lapse photography reveals the occurrence of unexpected bee- タイトル pollination in Calanthe izuinsularis, an endangered orchid endemic to Title the Izu archipelago 著者 Suetsugu, Kenji / Nakahama, Naoyuki / Ito, Azusa / Isagi, Yuji Author(s) 掲載誌・巻号・ページ Journal of Natural History,51(13-14):783-792 Citation 刊行日 2017-03-07 Issue date 資源タイプ Journal Article / 学術雑誌論文 Resource Type 版区分 author Resource Version This is an Accepted Manuscript of an article published by Taylor & 権利 Francis in Journal of Natural History on 07/03/2017 available online: Rights http://www.tandfonline.com/10.1080/00222933.2017.1293745 DOI 10.1080/00222933.2017.1293745 JaLCDOI URL http://www.lib.kobe-u.ac.jp/handle_kernel/90004565 PDF issue: 2021-10-01 1 Time-lapse photography reveals the occurrence of unexpected bee-pollination in 2 Calanthe izuinsularis, an endangered orchid endemic to the Izu archipelago 3 4 Kenji Suetsugu1*, Naoyuki Nakahama2, Azusa Ito2, Yuji ISAGI2 5 6 1Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, 7 Nada-ku, Kobe, 657-8501, Japan 8 2Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo- 9 ku, Kyoto, 606-8502, Japan 10 *Corresponding author Email [email protected] 11 12 Calanthe izuinsularis is a rare, beautiful and fragrant orchid endemic to the Izu 13 archipelago. Although it is known that mainland populations of closely related Calanthe 14 species are pollinated by medium- to large-sized bees, it is likely that C. izuinsularis has 15 been forced to alter its floral biology to attract alternative pollinators, as large-sized bees 16 are rarely found on the Izu Islands. Indeed, the unusual floral characteristics of C. 17 izuinsularis, which produces pale flowers that emit a strong and fragrant scent during the 18 night, are considered the adaptation to a moth-pollinator syndrome. As expected, our 19 time-lapse photography using a digital camera revealed that the inflorescences of C. 20 izuinsularis were most frequently visited by nocturnal moths such as Noctuidae, 21 Geometridae and Crambidae, which accounted for 50% of all insect visits (both in terms 22 of the number of frames with captured visitors and number of times visited). However, 23 our study could not provide evidence of a pollinator shift toward moths because none of 24 the moth species was observed with pollinaria. On the other hand, our study found that 1 1 the pollinaria of C. izuinsularis could become attached to the mesothorax of the small- 2 sized sweat bee Lasioglossum occidens. Therefore, our study suggested that C. 3 izuinsularis is still somewhat dependent on bee pollination, while the orchid has changed 4 its floral coloration and scent. The occurrence of bee-pollination in C. izuinsularis would 5 provide an explanation for how the natural hybridization between C. aristulifera, C. 6 discolor and C. izuinsularis can occur. 7 8 KEYWORDS insular endemic plant; island biology; orchid; pollinator shift; speciation 9 10 Introduction 11 The genus Calanthe (Orchidaceae) comprises approximately 200 species of primarily 12 terrestrial or lithophilic orchids distributed throughout Africa, Madagascar, China, Japan, 13 tropical Asia, and Australia (Karasawa & Ishida 1998). By far the greatest concentration 14 of the Calanthe species occurs on the islands of the Malay Archipelago (particularly 15 Borneo, Java, Sulawesi and Sumatra) and New Guinea. In addition, notable centers of 16 diversity also occur in the higher latitudes of Asia, in Indochina and subtropical China, 17 and in subtropical and temperate East Asia (Cribb & Bailes 2001; Gale & Drinkell 2007), 18 with approximately 30 species being found in Japan, the Korean Peninsula, and the 19 eastern provinces of China, including Taiwan (Govaerts et al. 2016). Calanthe 20 izuinsularis is a rare, beautiful and fragrant orchid endemic to the Izu archipelago, a chain 21 of islands extending from north to south near the main Japanese island of Honshu in the 22 west Pacific Ocean. Having been formed by volcanic activity, the Izu Islands have never 23 been connected with mainland Honshu (Karig 1975). C. izuinsularis is closely related to 24 three other species, Calanthe aristulifera, Calanthe discolor and Calanthe striata, which 2 1 are widely distributed throughout the islands of Japan (Cribb & Bailes 2001). The 2 similarity of C. izuinsularis to the other Calanthe species (especially C. aristulifera) 3 suggests that it could have evolved from a common ancestor, possibly as the result of a 4 few chances of seed dispersal events (Cribb & Bailes 2001). 5 The pollinator assemblage of oceanic islands is known to have reduced diversity 6 compared to similar habitats on the mainland (Carlquist 1974; Inoue & Amano 1986), 7 and it has been noted that in particular the insect faunas of oceanic islands often lack the 8 large-sized bees regarded as important pollinators on the mainland (Carlquist 1974; Inoue 9 & Amano 1986; Kato et al. 1999). It is therefore not surprising that large-sized bees are 10 rarely found on the Izu Islands, and with the exception of Oshima Island, bumblebees are 11 completely absent (Fukasawa & Miyano 2010). Consequently, it seems likely that the 12 impoverished pollinator assemblage could have affected the reproductive biology of the 13 flowering plants found there. Several studies have confirmed the corolla of bee-pollinated 14 plants on the Izu Islands tend to be smaller in size (Inoue & Amano 1986, Yamada et al. 15 2010; Yamada & Maki 2014; Yamada et al. 2014), possibly because of shifts in their 16 pollination strategy, such as attracting small-sized bees, including halictid bees, and/or 17 the acquisition of the capacity to self-fertilize. It is also possible that some plant species 18 on the Izu Islands have adapted to a moth-pollinator syndrome. For example, it has been 19 noted that in contrast to their mainland relatives, Weigela coraeensis var. fragrans and 20 Lilium auratum var. platyphyllum produce strongly scented flowers, which are 21 characteristic of moth-pollinated plants (Inoue 1990; Mizusawa et al. 2014). 22 Consequently, moths are considered important alternative pollinators on the Izu Islands 23 (Inoue 1990; Mizusawa et al. 2014). 24 Calanthe izuinsularis is a self-compatible, but pollinator-dependent orchid endemic 3 1 to the Izu archipelago (Karasawa & Ishida 1998). The flowers of C. izuinsularis, which 2 have a relatively long spur, pale coloration and a strong, fragrant scent emitted during the 3 night, suggest this species could also have co-opted moth pollinators (e.g. Giménez- 4 Benavides et al. 2007), instead of the bee pollinators utilized by its close relatives (C. 5 aristulifera, C. discolor and C. striata; Suhara 1993; Sugiura 2013; Suetsugu & 6 Fukushima 2014; Suetsugu et al. 2016). In spite of the expectation, there is no information 7 on its floral visitors in the natural habitat. We here investigated the floral visitor 8 assemblages of C. izuinsularis on Mikura Island, the Izu Islands. 9 10 Material and Methods 11 The study was primarily conducted using the interval-programming function of a 12 waterproof digital camera (Optio WG-1, Pentax, Japan). This approach has recently been 13 confirmed to be an effective substitute for direct observation of rare orchid pollination 14 events (Suetsugu & Tanaka 2013a, b; Suetsugu & Haymizu 2014). The study was 15 conducted on Mikura Island in the Tokyo Prefecture of Japan in early May 2012. Mikura 16 Island is one of the seven main islands of the Izu Islands group, which stretches south 17 from the entrance of the Bay of Tokyo. The island has an area of 20.55 km2 and is located 18 in the middle of the Izu Islands, approximately 200 km south of central Tokyo. 19 The camera was mounted on a flexible tripod (gorillapod, Joby, San Francisco) and 20 placed directly in front of individual C. izuinsularis specimens (ca. 30 cm away) so the 21 entire inflorescence was in focus. The camera was manually focused because the 22 automatic focus mode significantly shortened battery life. The camera was set to take 23 pictures automatically at 30- to 180-second intervals using an internal flash and batteries 24 (D-LI92 Pentax, Japan; Appendix 1), and the JPEG-format images were automatically 4 1 recorded onto an 8 GB SD card. We alternately photographed floral visitors per flowering 2 Calanthe from two or three angles to cover all the flowers and thus could obtain the 3 photographical data at ca. 10- to 60-second intervals (Appendix 1). Floral visitors were 4 defined as those species that not only were in the photographs, but also were attached to 5 the flowers. Pollinators were defined as those species that not only visited flowers, but 6 also carried pollinaria. The identities of the insect species captured by the time-lapse 7 photography were verified by insect taxonomists at the National Museum of Nature and 8 Science, Tokyo. 9 10 Results and Discussion 11 As expected by the unusual floral characteristics of C. izuinsularis, which produces pale 12 flowers that emit a strong and fragrant scent during the night, our study showed that 13 nocturnal moths were the most frequent visitors to the flowers of C. izuinsularis, 14 accounting for more than 50% of all insect visitors [in terms of both the number of frames 15 capturing visitors (247/442) and number of times visited (22/38; Table 1)]. In contrast, no 16 diurnal lepidopterans were observed throughout the entire duration of the investigation. 17 Furthermore, the assemblage of floral visitors differed dramatically in comparison to 18 closely related Calanthe species C. aristulifera, C. discolor and C. striata, which are 19 exclusively pollinated by bees and seldom visited by moths (Suhara 1993; Sugiura 2013; 20 Suetsugu & Fukushima 2014; Suetsugu et al. 2016). Indeed, intensive nighttime 21 observation covering 89 hours of time-lapse photography detected no nocturnal moth 22 visitors to the flowers of C.