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. discolor, even in the sympatric population of the present
23 investigation (Suetsugu et al. unpublished data). However, although most of the nocturnal
24 moths exhibited typical pollinator behavior, inserting their proboscises into the spur of
5
1 the C. izuinsularis flowers, no images of moths with C. izuinsularis pollinaria attached to
2 their proboscises were captured (Fig. 1). In some cases this might be have been expected,
3 as moth species such as Paliga minnehaha (Crambidae) are too small to carry the C.
4 izuinsularis pollinaria. In addition, the fact that no pollinaria transfer was observed with
5 the larger species Diarsia deparca (Noctuidae) and Serrodes campanus (Noctuidae) also
6 indicates that the frequency of pollinaria removal by these settling moths seems to be low,
7 if it even occurs. Therefore, the current study could not provide the evidence that
8 pollinator shifts toward nocturnal moths occur in C. izuinsularis in spite of the dominance
9 of moth floral visitors.
10 Although nocturnal moths were the most frequent visitors, there were also a
11 significant number of hymenopteran visitors, and in terms of the number of times visited
12 (8/38), they are the second-most frequent functional group of C. izuinsularis floral visitors.
13 All of the bee species observed visiting the flowers of C. izuinsularis exhibited typical
14 pollinator behavior, crawling deep into the chamber formed between the column and
15 labellum to forage for nectar (Fig. 1). Although the smaller bees (Lasioglossum
16 (Evylaeus) sp.) were unable to carry pollinaria, the sweat bee Lasioglossum occidens was
17 observed with pollinaria attached to its thorax (Fig. 1). Consecutive before and after
18 photographs indicated the bee had not been carrying any pollinaria when it arrived at the
19 flower and thus indicated that the attached pollinaria were truly derived from C.
20 izuinsularis, even though it cannot be absolutely certain how the pollinaria became
21 attached to its mesothorax. These results indicate that bee species could be an important
22 pollinator of C. izuinsularis, while the floral characteristics of these species, such as
23 perianth size, perianth color, and fragrance of C. izuinsularis, seem adapted to different
24 pollinator assemblages. Furthermore, this small bee pollination system could also provide
6
1 an explanation for the natural hybrids of C. izuinsularis and C. discolor that have been
2 found on the islands of Kohzu, Nii and Hachijo, as well as the hybrids of C. izuinsularis
3 and C. aristulifera found on Mikura Island, the site of the current study (Cribb & Bailes
4 2001). Indeed, a previous study of a sympatric C. aristulifera population at the current
5 study site found that C. aristulifera was also pollinated by L. occidens (Suetsugu et al.
6 2016). Given that C. aristulifera and C. discolor are rarely visited by nocturnal moths
7 (Suhara 1993; Sugiura 2013; Suetsugu & Fukushima 2014; Suetsugu et al. unpublished
8 data), the weight of evidence suggests that pollination by hymenopteran floral visitors is
9 the most likely mechanism of hybridization between C. izuinsularis, C. discolor and C.
10 aristulifera.
11 It is also interesting to note that the pollinaria of C. izuinsularis were attached to
12 the mesothorax of the sweat bees, as is also the case for C. aristulifera (Suetsugu et al.
13 2016). This is in contrast to the mechanism of pollination found in all the mainland
14 Calanthe populations investigated to date, which involves the heads of pollinating bees
15 pushing against the tip of the column and the pollinaria becoming attached to a narrow
16 region between the supraclypeal area and the vertex of the head, or if already laden, being
17 transferred to the stigmatic surface when they insert their proboscises into the spur
18 (Sugiura 2013; Suetsugu & Fukushima 2014). A similar mechanism of transfer cannot
19 occur with sweat bees because their smaller size prevents their heads from making contact
20 with the tip of the column. Instead, pollinaria can only be transferred when the bee crawls
21 deep into the spur and the anthers make contact with the mesothorax. It is also likely that
22 this alternative mechanism of pollination in both C. izuinsularis and C. aristulifera arose
23 on Mikura Island by convergent evolution in response to the lack of bumblebees and other
24 relatively large bees, such as the genus Eucera (Fukasawa & Miyano 2010).
7
1 Overall, we found that C. izuinsularis attracts a different assemblage of insect
2 visitors from its close relatives, C. discolor and C. aristulifera. However, although the
3 majority of floral visitors were moths, we could not provide any evidence that pollinator
4 shifts toward nocturnal moths occur in C. izuinsularis. The small sweat bee Lasioglossum
5 occidens is the only demonstrable pollinator of C. izuinsularis in the present study. This
6 apparent disconnect between pollination syndrome and pollinator species is unexpected
7 and warrants further study. Investigating detailed reproductive biology could be an
8 important next step to understand the pollination efficiency and importance on the
9 evolution of floral traits of each floral visitor.
10 It should be noted that the interval photography used in the current study could
11 have underestimated the role of some visitor groups that are quick in their approach and
12 resource collection. For example, the frame rate used in the current study might have been
13 insufficient to detect hawkmoths (Sphingidae), which are known to hover in front of
14 inflorescence and only make brief visits (Steen 2012). Considering these facts, our limited
15 study does not exclude the possibilities of moth pollination (especially hawkmoth
16 pollination). Some plants are known to utilize different types of pollinators, increasing
17 the chance of pollination (Giménez-Benavides et al. 2007, Li et al. 2010, Amorim et al.
18 2013). For example, Giménez-Benavides et al. (2007) showed that diurnal flower visitors
19 have frequently been recorded, and can provide greater fitness in Silene ciliata while S.
20 ciliata, with pale flowers that open at dusk and emit an intense scent at night, presents a
21 typical nocturnal pollination syndrome. C. izuinsularis may also utilize both moth and
22 bee pollinators to maximize its pollination efficiency. Further investigations utilizing
23 continuous video monitoring, event-triggered video monitoring or direct observation are
24 therefore required to accurately document the pollinator assemblage of C. izuinsularis
8
1 and identify the most effective pollinator of this insular endemic Calanthe species (e.g.
2 Steen 2012, Steen & Mundal 2013). In addition, it is worth investigating why C.
3 izuinsularis attract moth floral visitors recorded in the present study if these moths truly
4 do not work as the pollinators.
5
6 Acknowledgements
7 We thank Mr. Masayuki Hino for his assistance during the field study. We also thank Drs.
8 Utsugi Jinbo and Yuta Nakase for their help with identifying floral visitors. We gratefully
9 acknowledge the sponsorship and the support of the New Technology Development
10 Foundation and the grant-in-aid by the Japan Society for the Promotion of Science
11 (15K18470).
12
13 References
14 Amorim FW, Galetto L, Sazima M. 2013. Beyond the pollination syndrome: nectar
15 ecology and the role of diurnal and nocturnal pollinators in the reproductive success
16 of Inga sessilis (Fabaceae). Plant Biol. 15:317–327.
17 Carlquist S. 1974. Island Biology. Columbia University Press, New York.
18 Cribb P, Bailes C. 2001. Calanthe izuinsularis. Curtis's Botanical Magazine. 18:101–
19 103.
20 Gale S, Drinkell C. 2007.Calanthe arisanensis. Curtis's Botanical Magazine. 24:206–
21 210.
22 Fukasawa S, Miyano S. 2010. Fauna of the aculeate Hymenoptera (Insecta) from the Izu
23 Islands, Japan. J Nat Hist Mus Inst Chiba. 11:11–28.
24 Giménez Benavides L, Dötterl S, Jürgens A, Escudero A, Iriondo JM. 2007. Generalist
9
1 diurnal pollination provides greater fitness in a plant with nocturnal pollination
2 syndrome: assessing the effects of a Silene–Hadena interaction. Oikos. 116:1461–
3 1472.
4 Govaerts R, Bernet P, Kratochvil K, Gerlach G, Carr G, Alrich P, Pridgeon AM, Pfah J,
5 Campacci MA, Holland Baptista D, Tigges H, Shaw J, Cribb PJ, George A, Kreuz K,
6 Wood JJ. 2016. World Checklist of Orchidaceae. Facilitated by the Royal Botanic
7 Gardens, Kew. (accessed on 31 January 2016).
8 Inoue K. 1990. Relationships between plants and pollinators on the Izu Islands. The
9 Natural History of Japan. 4:26–33.
10 Inoue K, Amano M. 1986. Evolution of Campanula punctate Lam. in the Izu Islands:
11 change of pollinators and evolution of breeding systems. Plant Species Biol. 1:89–97.
12 Inoue K, Maki M, Masuda M. 1995. Evolution of Campanula flowers in relation to
13 insect pollinators on islands. In: Lloyd DG, Barrett SCH (eds) Floral biology.
14 Chapman and Hall, New York, 377–400 pp.
15 Kato M, Shibata A, Yasui T, Nagamasu H. 1999. Impact of introduced honeybees, Apis
16 mellifera, upon native bee communities in the Bonin (Ogasawara) Islands. Res Popul
17 Ecol. 41:217–228.
18 Karig DE. 1975. Basin genesis in the Philippine sea. In: Karig DE, Ingle JC (eds) Initial
19 reports of the deep sea drilling project 31. United States Government Printing Office,
20 Washington, DC, 857–879 pp.
21 Karasawa K, Ishida G. 1998. The genus Calanthe. Yasaka Shobo, Tokyo.
22 Li P, Zheng GL, Dafni A, Luo YB. 2010. Reproductive biology of an alpine orchid
23 Phaius delavayi. Plant Syst Evol. 286:167–173.
24 Mizusawa L, Takimoto G, Yamasaki M, Isagi Y, Hasegawa M. 2014. Comparison of
10
1 pollination characteristics between the insular shrub Clerodendrum izuinsulare and its
2 widespread congener C. trichotomum. Plant Species Biol. 29:73–84.
3 Neiland MRM, Wilcock CC. 1998. Fruit set, nectar reward, and rarity in the
4 Orchidaceae. Am J Bot. 85:1657–1671.
5 Philipp M, Böcher J, Siegismund HR, Nielsen LR. 2006. Structure of a plant–pollinator
6 network on a pahoehoe lava desert of the Galápagos Islands. Ecography. 29:531–540.
7 Steen R. 2012. Pollination of Platanthera chlorantha (Orchidaceae): new video
8 registration of a hawkmoth (Sphingidae). Nord J Bot. 30:623–626.
9 Steen R, Mundal D. 2013. New video registration of Autographa pulchrina (Haworth,
10 1809)(Lepidoptera, Noctuidae) and Sphinx pinastri L., 1758 (Lepidoptera,
11 Sphingidae) pollinating Platanthera bifolia latiflora (Orchidaceae) in Norway. Norw
12 J Entomol. 60:57-61.
13 Suetsugu K, Fukushima S. 2014. Bee pollination of the endangered orchid Calanthe
14 discolor through a generalized food-deceptive system. Plant Syst Evol. 300:453–459.
15 Suetsugu K, Hayamizu M. 2014.Moth floral visitors of the three rewarding orchids
16 Platanthera revealed by interval photography with a digital camera. J Nat Hist.
17 48:1103–1109.
18 Suetsugu K, Tanaka K. 2013. Moths visiting the flowers of orchid Platanthera japonica.
19 Entomol News. 123:78–80.
20 Suetsugu K, Tanaka K. 2013. Pollination of Sedirea japonica (Orchidaceae) by Bombus
21 diversus diversus (Hymenoptera: Apidae). Eur J Entomol. 110:545–548.
22 Suetsugu K, Nakahama N, Ito A, Hino M, Isagi Y. 2016. The sweat bee Lasioglossum
23 occidens is a potential pollinator of Calanthe aristulifera in the oceanic Izu Islands.
24 Entomol News in press.
11
1 Sugiura N. 2013. Specialized pollination by carpenter bees in Calanthe striata
2 (Orchidaceae), with a review of carpenter bee pollination in orchids. Bot J Linn Soc.
3 171:730–743.
4 Suhara K. 1993. Classification of the spring-flowering Calanthe with special reference
5 to their floral visitors. Engei Mania 3:20–23.
6 Yamada T, Kashiwagi T, Sawamura M, Maki M. 2010. Floral differentiation among
7 insular and mainland populations of Weigela coraeensis (Caprifoliaceae). Plant Syst
8 Evol. 288: 113–125.
9 Yamada T, Kodama K, Maki M. 2014. Floral morphology and pollinator fauna
10 characteristics of island and mainland populations of Ligustrum ovalifolium
11 (Oleaceae). Bot J Linn Soc. 174:489–501.
12 Yamada T, Maki M. 2014. Relationships between floral morphology and pollinator
13 fauna in insular and main island populations of Hosta longipes (Liliaceae). Plant
14 Species Biol. 29:117–128.
15
16
17
18
19
20
21
22
23
24
12
1 Table 1. List of floral visitors recoreded using interval photography. Numbers given are the total numbers of frames recording visitors, and times visited. Frames with Times Pollinalia No. Photographed species Order visitors captured visited attached 1 Lasioglossum occidens Hymenoptera 26 6 Yes 2 Lasioglossum (Evylaeus) sp. Hymenoptera 4 2 No 3 Calliphoridae sp. Diptera 7 2 No 4 Tipulidae sp. Diptera 80 2 No 5 Cyclorrhapha sp. Diptera 5 2 No 6 Paliga minnehaha Lepidoptera 36 4 No 7 Diarsia deparca Lepidoptera 35 7 No 8 Geometridae Ennominae sp. Lepidoptera 5 1 No 9 Geometridae sp. Lepidoptera 7 1 No 10 Geometridae Larentiinae sp. Lepidoptera 1 1 No 11 Geometridae or Noctuidae sp. Lepidoptera 8 1 No 12 Noctuidae. sp. Lepidoptera 1 1 No 13 Noctuidae Plusiinae sp. Lepidoptera 2 1 No 14 Odontopera arida melanchonica Lepidoptera 137 2 No 15 Photoscotosia lucicolens Lepidoptera 12 1 No 16 Serrodes campanus Lepidoptera 2 1 No 17 Thysanoplusia intermixta Lepidoptera 1 1 No 18 Tettigoniidae sp. (nymphs) Orthoptera 73 2 No
2
3
4
5
13
1
2 Figure 1. Flowers and insect visitors of Calanthe izuinsularis. (A) Photoscotosia
3 lucicolens; (B) Odontopera arida melanchonica; (C) Noctuidae sp.; (D) Geometridae sp.;
4 (E) Trichoplusia intermixta; (F) Diarsia deparca; (G) Paliga minnehaha; (H) Serrodes
5 campanus; (I) Lasioglossum apristum; (J) Lasioglossum occidens; (K) Lasioglossum
6 occidens. The pollinaria indicated by white arrows can be seen attached to the bee’s
7 mesothorax.
14