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Generalist Pollinators in the Dioecious Shrub Rhus Trichocarpa Miq

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Generalist Pollinators in the Dioecious Shrub Rhus Trichocarpa Miq Plant Species Biology (2009) 24, 215–224 doi: 10.1111/j.1442-1984.2009.00258.x NOTES AND COMMENTS Generalist pollinators in the dioecious shrub Rhus trichocarpa Miq. (Anacardiaceae) and their role in reproductive successpsbi_258 215..224 SHUHEI MATSUYAMA,* NAOYA OSAWA† and MICHINORI SAKIMOTO‡ *Laboratory of Silviculture, Division of Forest and Biomaterials Science, †Laboratory of Forest Ecology, Graduate School of Agriculture and ‡Laboratory of Forest Species and Ecosystem Conservation, Field Science Education and Research Center, Kyoto University, Kyoto 606-8503, Japan Abstract We examined the floral display size and potential pollinators of female and male Rhus trichocarpa in northern Kyoto, Japan, in June 2005. The entomophilous pollination system comprised 431 insects and one spider belonging to 124 species. Most pollinators were non-social bees and occasional Diptera and Coleoptera, whereas eusocial bees were not dominant in the pollination system. Male-biased frequencies were observed in the eusocial bees and in some of the non-social bees, probably because they are sensitive to the larger male floral rewards. A pollinator introduction experiment confirmed that male- biased, unbiased and infrequent non-social bees can pollinate R. trichocarpa, indicating that non-social bees can contribute to fruit set. The results suggest that there are likely to be two different functional groups of generalist pollinators: (i) the majority of the polli- nators may contribute to reproductive success through unbiased and occasional visits; and (ii) a minority group of eusocial bees may contribute to reproductive success through male-biased visits. Keywords: dioecy, floral display size, generalist pollinator, Rhus trichocarpa, visitation frequency. Received 1 May 2009; accepted 13 July 2009 Introduction Pollinators, including generalists, usually use floral rewards from plants. Several studies have shown that pol- Interaction with pollinators is a determining factor in linators will visit plants with larger floral rewards more entomophilous plant reproductive success; reproductive frequently than those with smaller rewards (e.g. Huang success depends on the availability of resources for et al. 2006). However, the frequency of visits to focal allocation into plant reproductive organs and on the effec- plants differs among pollinator species (Ågren et al. 1986; tiveness of pollen transfer by animal vectors. Most Farwig et al. 2004; Voigt et al. 2005). Some studies indicate entomophilous interaction studies have focused on the that individual plant species enhance their reproductive relationships between plants and specialist pollinators success through interactions with many species of (e.g. Kevan & Baker 1983) or frequent generalist pollina- frequent and infrequent generalist pollinators (e.g. tors, such as eusocial bees (e.g. Mitchell et al. 2004; Hira- Schemske & Horvitz 1984; Dukas 1987). bayashi et al. 2006). Recent theoretical studies suggest that Many dioecious plant species are believed to be polli- plants may favor generalist as well as specialist pollinators nated mainly by generalist pollinators, such as eusocial (Waser et al. 1996; Aigner 2001; Sargent & Otto 2006). and solitary bees, flies, other Diptera and Coleoptera (e.g. However, generalist pollinator interactions with plants Opler et al. 1980; Muenchow 1987). In addition, dioecious are less well documented. plant pollination is believed to be more efficient than that in hermaphrodite species (Sutherland & Delph 1984). Correspondence: Shuhei Matsuyama Thus, dioecy and/or the generalist-dominant pollinator Email: [email protected] syndrome contribute to highly efficient pollination © 2009 The Authors Journal compilation © 2009 The Society for the Study of Species Biology 216 S. MATSUYAMA ET AL. success (i.e. reproductive success). However, the precise with numerous small flowers (Ohwi & Kitagawa 1992). mechanisms elevating reproductive success in these cases Most flower corollas are <10 mm wide and <10 mm tall (S. are unclear because solitary bees, flies, other Diptera and Matsuyama, 2005). In the study area flowering occurs in Coleoptera are believed not to transfer pollen as effec- early June and fruits mature in October (Matsuyama & tively as eusocial bees (e.g. bumble bees), which some Sakimoto 2008). The sexes of R. trichocarpa flowers can dioecious plants use as their preferred pollinators in be distinguished by color; male flowers are yellowish nature (Thomson et al. 1982; Dukas 1987; Herrera 1989). and female flowers are greenish (S. Matsuyama, unpubl. Several empirical studies have demonstrated that the data, 2001). Male flowers produce both pollen and pollination systems of dioecious species are characterized nectar, whereas female flowers produce only nectar in by biased pollinator visits to male plants because of R. trichocarpa (S. Matsuyama, unpubl. data, 2005). elevated rewards in their flowers (e.g. Ågren et al. 1986; Bierzychudek 1987; Elmqvist et al. 1988). However, Visitor fauna and visitation frequency extremely male-biased visits in dioecious plants may lead to pollen loss and to a reduction in reproductive success In 2005, we randomly selected 20 flowering plants (9 (Charlesworth 1993). Hence, a non-bias in the frequency of male, 11 female) and recorded visitation fauna, visitation visits may play a certain role in the reproductive success of frequency, floral display size and fruit set. dioecious plants in addition to the frequency of visits. To examine visitor fauna and visitation frequency in R. Rhus trichocarpa (Anacardiaceae) is a common ento- trichocarpa, flower visitors to female (n = 11) and male mophilous dioecious shrub that favors disturbed sites in plants (n = 9) were captured on fine weather days in the temperate zone of Japan (Kamitani et al. 1998; Osada June 2005 (from nine plants on 9 June, six plants on 10 2005). Flowers of Rhus spp. are visited by several species June and five plants on 14 June). Fine weather days were of bees, flies and other insects (Kato et al. 1990), suggest- chosen because there is a negative effect of rain on the ing that many generalist pollinators influence the repro- number of visitors. For each plant, one reproductive ductive success of the plants. current-year shoot with open flowers was selected and The objectives of the present study were to determine all arthropods on inflorescences of the shoot were caught the effects of visits by many generalist pollinators on the over 15 min. For the first 12 min all of the visitors were reproductive success of R. trichocarpa in a primary beech caught with a net, after that an aspirator was used for the forest in Japan by: (i) identifying all potential pollinators to last 3 min. This sampling was repeated five times per the species level; (ii) evaluating floral display size and fruit day for the same shoot on each plant, from approxi- set; and (iii) evaluating the pollination efficiency of selected mately 08.00–13.00 hours at 45-min intervals. potential pollinators using an introduction experiment. All visitor samples were pinned and labeled with com- plete census data (date, locality and flower type). Visitors were classified to the species level where possible. Three Materials and methods hundred and thirty-eight individuals, 78.2% of the total, were identified to species. The remaining individuals (95) Study site and target species were assigned to higher taxa (generally family). All speci- The study was conducted in 2005 at the Asiu Forest mens were deposited in the Laboratory of Silviculture, Research Station of Kyoto University in the northern part Graduate School of Agriculture, Kyoto University. of Kyoto Prefecture, western Japan (35°18′N, 135°43′E; One dataset of visits per 15 min for all visitor species 750 m a.s.l.). The mean annual air temperature and annual and each plant (5 collection times ¥ 124 species ¥ 20 precipitation at a nearby weather station are 11.9°C and plants = 12 400 data points) was constructed. The average 2298.3 mm, respectively (Kyoto University Field Science visitation frequency per 15 min was calculated for each Education Research Center 2007). The study area is a species and for the total species and was compared among natural conifer/hardwood forest dominated by the ever- arthropod orders. For each order, the average visitation green conifer Cryptomeria japonica and the deciduous frequency was compared among species captured on broadleaf species Fagus crenata, Acer sieboldianum and female and male plants. The difference between plant Quercus crispula (see Hirayama & Sakimoto 2003). sexes was examined as the average visitation frequency Rhus trichocarpa is native to the mountains and foothills for the total species, and for the species captured on both of north-eastern Asia: Japan, including the southern female and male plants. Kuriles, Hokkaido, Honsyu, Shikoku, Kyusyu and Okinawa; Korea; and China (Ohwi & Kitagawa 1992). It is Floral display size a deciduous shrub approximately 4 m in height in the study area (Matsuyama & Sakimoto 2008). The inflores- To evaluate the display size of female and male flowers cence forms from axillary buds on current-year shoots, we calculated the number of flowers per plant by multi- © 2009 The Authors Plant Species Biology 24, 215–224 Journal compilation © 2009 The Society for the Study of Species Biology POLLINATION SYSTEM OF RHUS TRICHOCARPA 217 plying the number of reproductive current-year shoots introduced onto female inflorescences enclosed in bags per plant by the number of inflorescences per shoot and and fruiting
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