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Kobe University Repository : Kernel Kobe University Repository : Kernel Relative importance of diurnal and nocturnal pollinators for タイトル reproduction in the early spring flowering shrub Stachyurus praecox Title (Stachyuraceae) 著者 Funamoto, Daichi / Sugiura, Shinji Author(s) 掲載誌・巻号・ページ Plant Species Biology,36(1):94-101 Citation 刊行日 2021-01 Issue date 資源タイプ Journal Article / 学術雑誌論文 Resource Type 版区分 publisher Resource Version © 2020 The Authors. Plant Species Biology published by John Wiley & Sons Australia, Ltd on behalf of Society for the Study of Species 権利 Biology. This is an open access article under the terms of the Creative Rights Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. DOI 10.1111/1442-1984.12299 JaLCDOI URL http://www.lib.kobe-u.ac.jp/handle_kernel/90007882 PDF issue: 2021-10-05 Received: 23 April 2020 Revised: 7 August 2020 Accepted: 12 September 2020 DOI: 10.1111/1442-1984.12299 ORIGINAL ARTICLE Relative importance of diurnal and nocturnal pollinators for reproduction in the early spring flowering shrub Stachyurus praecox (Stachyuraceae) Daichi Funamoto | Shinji Sugiura Graduate School of Agricultural Science, Kobe University, Kobe, Japan Abstract Generalized pollination systems may be favored in early spring flowering Correspondence plants, as during this period pollinator activity is unpredictable. Many previous Daichi Funamoto, Graduate School of Agricultural Science, Kobe University, 1-1 studies have concentrated on the importance of diurnal visitors in pollination, Rokkodai, Nada-ku, Kobe 657-8501, and consequently, information on the contribution of nocturnal visitors to pol- Japan. lination in early spring is limited. This study was conducted to evaluate the rel- Email: [email protected] ative importance of diurnal and nocturnal pollinators in the early spring Funding information flowering dioecious shrub Stachyurus praecox (Stachyuraceae), in two temper- Japan Society for the Promotion of ate forests in central Japan. Visitors to the female and male flowers were Science, KAKENHI, Grant/Award Number: 18J20388; Japan Science Society, observed during day and night, and their relative contributions to seed set Sasakawa Scientific Research, Grant/ were compared. The pollinator observations revealed that the diurnal and noc- Award Number: 29-544 turnal insects visited both male and female flowers, and that the main flower visitors were diurnal small bees and flies as well as nocturnal settling moths. The diurnal and nocturnal flower visitors also acted as pollinators, as the pol- len grains of S. praecox were attached to the insects collected from the female flowers. Pollination experiments demonstrated that the contributions of diur- nal pollinators to the seed set were higher than those of the nocturnal pollina- tors. The results of this study indicate that S. praecox has a generalized pollination system, comprising both diurnal insects and nocturnal settling moths. Although the roles of diurnal insects are more important in the pollina- tion of S. praecox, nocturnal settling moths may have a complementary role in early spring. KEYWORDS Andrenidae, functional dioecy, gynodioecy, moth pollination, Noctuidae 1 | INTRODUCTION Klein, 2011; Macgregor, Pocock, Fox, & Evans, 2019). Generalized pollination systems are widespread in angio- Plants pollinated by multiple groups of animals might sperms (Funamoto, 2019; Leal et al., 2020; Waser, have advantages because different groups of pollinators Chittka, Price, Williams, & Ollerton, 1996). These polli- can be complementary to each other (Blüthgen & nation systems are frequently found in environments This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Plant Species Biology published by John Wiley & Sons Australia, Ltd on behalf of Society for the Study of Species Biology 94 wileyonlinelibrary.com/journal/psbi Plant Species Biol. 2021;36:94–101. FUNAMOTO AND SUGIURA 95 such as oceanic islands (Kaiser-Bunbury, Traveset, & Nocturnalmoths,aswellasdiurnalinsects,areknown Hansen, 2010; Weissmann & Schaefer, 2017) and high to visit several early spring flowers, such as Daphne mountains (Freitas & Sazima, 2006; Peng, Zhang, Xu, laureola (Thymelaeaceae), Narcissus spp. (Amaryllidaceae), Li, & Sun, 2012), where pollinator availability is Pieris japonica (Ericaceae), Salix caprea (Salicaceae) and unpredictable. In addition, generalized pollination sys- Stachyurus praecox (Stachyuraceae) (Abe, 2007; tems may be favored in early spring flowering plants Alonso, 2004; Ikenoue, 1990; Ikenoue & Kanai, 2010; (Alonso, 2004; Rosati et al., 2019). Pollination success in Jürgens, Glück, Aas, & Dötterl, 2014; Osada, Sugiura, early spring could be limited by several factors Kawamura, Cho, & Takeda, 2003; Pérez-Barrales, Vargas, & (Kudo, 1995; Kudo & Cooper, 2019). Firstly, the weather Arroyo, 2006). Plants often achieve maximum pollination in early spring is variable, and thus pollinator activity is success when pollinated by both diurnal and nocturnal pol- unpredictable (Motten, 1986). Secondly, low air tempera- linators (Amorim, Galetto, & Sazima, 2013; Macgregor tures in early spring can strongly restrict pollinator activ- et al., 2019). Therefore, nocturnal moths may play an ity (Herrera, 1995; Kudo, 1995). Furthermore, warm important role in the pollination of early spring flowers. springs can cause phenological mismatch between polli- However, the contribution of nocturnal moths to pollina- nator emergence and flowering (Kudo & Cooper, 2019). tion has been experimentally examined in only two species Many studies have shown that early spring flowering ofearlyspringfloweringplants,D. laureola and S. caprea plants are pollinated by a taxonomically diverse group of (Alonso, 2004; Jürgens et al., 2014). These studies have diurnal insects, such as bumblebees, small solitary bees, shown that nocturnal moths do not contribute to seed pro- bee flies and hoverflies (Dupont & Kato, 1999; duction in D. laureola and S. caprea (Alonso, 2004; Jürgens Motten, 1986; Sugiura, 2012; Wong Sato & Kato, 2017). et al., 2014), as S. caprea was found to be pollinated by bees However, relatively few studies have investigated the rel- and the wind (Jürgens et al., 2014), and D. laureola by ative contribution of different types of pollinators to polli- nitidulid beetles (Alonso, 2004). Thus, the roles of noctur- nation in early spring flowering plant species (Huang, nal settling moths in the pollination of early spring Song, & Huang, 2017). flowering plants remain poorly understood. FIGURE 1 Stachyurus praecox flowers and flower visitors: (a) a male plant in bloom; (b) an andrenid bee visiting male flowers with pollen grains attached to the face, legs and thorax; (c) a small bee visiting female flowers; (d) Bombylius major visiting male flowers; (e) a hoverfly, Criorhina sp., visiting male flowers with clumps of pollen grains attached to its face and legs; (f) Egira saxea visiting female flowers; (g) Goniocraspidum pryeri visiting male inflorescences; (h) G. pryeri visiting male flowers, pollen on the proboscis is indicated by the white arrow. (a) to (f) were taken at Ashiu, and (g) and (h) were taken at Takedao 96 FUNAMOTO AND SUGIURA This investigation was conducted to evaluate the rela- and from 2017 to 2019, in Takedao and Ashiu, respec- tive roles of the diurnal and nocturnal pollinators of tively. A female or male tree of S. praecox was selected Stachyurus praecox, a shrub that flowers in early spring from approximately 10 flowering trees and watched care- (Figure 1a). The flowers of S. praecox attract diverse fully during each observation. Diurnal observations were insects, including small bees, hoverflies and bee flies dur- performed on sunny days between 9:00 a.m. and 5:00 p. ing the day (Abe, 2007), whereas settling moths visit the m., at temperatures of 4–21C, whereas nocturnal obser- flowers at night (Ikenoue, 1990; Ikenoue & Kanai, 2010). vations were performed for 4 h after sunset (start time: Thus, both diurnal and nocturnal pollinators may be 6:00–6:33 p.m.) at temperatures of 4–14C. If no flower involved in the pollination of flowers. However, the rela- visitors were observed throughout the diurnal observa- tive contributions of diurnal and nocturnal pollinators to tions or within 1 h after sunset during the nocturnal the seed production of S. praecox have not previously observations, the data were excluded from the study as been investigated. This study aims to address the follow- this was an indication that the weather conditions may ing question. (a) Do both diurnal insects and nocturnal have been inappropriate for pollinator activity. Our pre- moths visit flowers across years and sites? (b) Are both liminary observations revealed that most of the nocturnal diurnal and nocturnal flower visitors carrying pollen flower visitors were active on flowers within 1 h after grains of S. praecox? (c) Do both diurnal and nocturnal sunset. flower visitors contribute to the seed production of The number of insects visiting inflorescences (height S. praecox? 1.5–3.0 m) on a S. praecox tree was recorded during each observation. The numbers of flowers observed on the female and male plants were 286.0 ± 131.6 (mean ± SD, 2 | MATERIALS AND METHODS n = 5) and 741.0 ± 809.5 (n = 7) in Ashiu, and 407.4 ± 152.3 (n = 5) and 418.8 ± 122.7 (n =5)in 2.1 | Species and sites Takedao,
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