COMPARISON OF FORAGING ACTIVITY BETWEEN MASON BEE OSMIA ORIENTALIS
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1 Volume 125, Number 5, March COMPARISON OF FORAGING ACTIVITY BETWEEN MASON BEE OSMIA ORIENTALIS (HYMENOPTERA: MEGACHILIDAE) AND HONYBEES FOR WILD RASP- BERRY RUBUS HIRSUTUS (ROSALES: ROSACEAE) 1 Tomoyuki Yokoi 2 and Ikuo Kandori 3 ABSTRACT: Foraging traits of honeybees and Osmia bees have previously been compared in crop production. However, less is known about the difference in foraging traits during visits to wild flowers. We conducted experiments to clarify the foraging behavior of Osmia orientalis visiting wild raspberry Rubus hirsutus and compared it with two solitary bees (Micrandrena spp. and Ceratina flavipes) and two honeybee species (Apis mellifera and A. cerana japonica). The average number of visiting individuals of O. orientalis was greater than that of honeybees. For O. orientalis, the handling time and the number of flowers that an individual visited were no different from those of honeybees. However, more O. orientalis individuals than honeybees collected pollen. The study suggests that the foraging activity of O. orientalis for wild raspberry would be as high as that of honeybees. KEY WORDS: Handling time, honeybee, Megachilidae, visitation frequency The Mason bee Osmia orientalis Benoist (Hymenoptera: Megachilidae) is one of seven Osmia species in Japan (Maeta and Miyanaga, 1999). Osmia bees visit the same floral resources as social honeybee species, such as the European honeybee Apis mellifera L. and Japanese honeybee A. cerana japonica Radosz kow - ski in Japanese rural environment, Satoyama (Miyamoto, 1959a, b). A comparison of the foraging traits between honeybee and Osmia bees was conducted in fruit trees, where Osmia bees were shown to be effective pollinators and seed set compared to honeybees (Maeta and Kitamura, 1981; Bosch and Blas, 1994; Sampson and Cane, 2000; Vicens and Bosch, 2000; Monzón et al., 2004; Cane, 2005). However, previous studies have not compared the foraging traits of these bees when they visit wild flowers. Here, we present a study of the foraging be - havior of O. orientalis Benoist visiting wild raspberry Rubus hirsutus Thunb. Raspberry R. hirsutus flowers in early spring, and the flowering season coincides with the occurrence of solitary bees including several Osmia bees. We examined whether the foraging pattern of the female, i.e. handling time and the number of sequential flower visits, differs from that of honeybees and other solitary bees. MATERIALS AND METHODS All experiments were conducted on the Nara campus of Kindai University, Nara, Japan (34º40'N, 135º43'E). We selected a wild raspberry community on the 1 Received on August 21, Accepted on November 18, Laboratory of Conservation Ecology, Faculty of Life and Environmental Sciences, University of Tsukuba, Tennodai, Tsukuba City, Ibaraki , Japan. Corresponding author. tomoyoko@envr.tsukuba.ac.jp 3 Laboratory of Entomology, Faculty of Agriculture, Kindai University, Nakamachi, Nara City, Nara, Japan Mailed on April 13, 2016
2 364 ENTOMOLOGICAL NEWS campus that was located on the roadside near a storage reservoir. The flowering area was approximately 750 m 2, re spectively, and each site was considered to be one clump. Four observation plots, each of which (1x1 m) was compartmented by using white vinyl rope, were randomly selected. Before the experiments, the number of flowers in each observation plot was manipulated to minimize floral variation. That is, we set ap prox imately 45 flowers (specifically, 40 50) in full bloom (within 2 days of open ing) per observation plot by either cutting or adding flowers. We added flowers to the observation plots by bending a long branch with flowers. The main bee visitors of R. hirsutus were five species: A. mellifera, A. c. japonica, O. orientalis, Micrandrena spp. and Ceratina flavipes. Except for the two honeybees, the other visiting species were solitary bees that occur in the spring season and visit several wild flowers. The five bee species were classified into two groups according to their body size, i.e. large bees (A. mellifera, A. c. japonica, and O. orientalis) and small bees (Micrandrena spp. and C. flavipes). The observations of handling time and foraging patterns were conducted be tween 0900 and 1400 h on 3 days, i.e. 30 April, 1 May, and 3 May, at site B in The observations of the number of sequential flower visits were conducted on 2 days at site B, i.e. 30 April and 1 May First, flower-visiting behavior of an individual was categorized to one of three foraging types: nectar-only foragers, which collected nectar only from flowers; pollen-only foragers, which collected pollen only; and pollen-nectar foragers, which collected both pollen and nectar. Then, the handling time per flower for each bee was recorded. This was defined as the time from landing on the flower to leaving after the collection of floral resources. The number of sequential flower visits for each bee was also counted. The counting started when an individual bee entered the observation plot and visited a flower, and ended when the bee left the observation plot. A Steel-Dwass test was used to compare the foraging time and the number of se quen tial flower visits between bee species. A Fisher s exact probability test was used to compare the ratio of pollen foragers and nectar-only foragers be - tween bee species. Pollen foragers included both pollen-only foragers and pollen-nectar foragers because these foraging types contributed to the pollination of wild raspberry. After each test, a sequential Bonferroni correction was used to deal with the increase in type I errors through multiple pair-wise comparisons (Rice, 1989). RESULTS and DISCUSSION The flower handling time of O. orientalis did not differ from that of A. mellifera and A. c. japonica (Fig. 1a). The handling time of these three large bee species was significantly shorter than that of the two small bees: Micrandrena spp. and C. flavipes (p <0.01, Steel-Dwass test). Handling time of three large bees was within 7 seconds while that of Micrandrena spp. and C. flavipes was ± 2.02 and ± 5.46, respectively. When considering the number of
3 Volume 125, Number 5, March Fig. 1. Comparison of the handling time per flower (a) and the number of sequential flower visits per individual among visiting bee species (b) Each bar represents the mean ± SE. Different letters indicate significant differences (Steel-Dwass test, p < 0.05).
4 366 ENTOMOLOGICAL NEWS Fig. 2. Percentage of female individuals that foraged nectar and/or pollen during visits to flowers. Different letters indicate significant difference in the ratio of (pollen-only foragers + pollen-nectar foragers) : (nectar-only foragers). (Fisher s exact probability test, p < 0.05.) sequential flower visits (Fig. 1b), the three large bees visited more flowers than two small bees did (p < 0.01, Steel-Dwass test). Most frequent flower visitor was A. c. japonica (7.68 ± 1.07 flowers), followed by A. mellifera (6.04 ± 0.53) and O. orientalis (5.05 ± 0.44). Two small bees, Micrandrena spp. and C. flavipes, were less frequent flower visitors. The number of sequential flowers visited by O. orientalis was similar to that by A. mellifera (p = 0.248, Steel-Dwass test), whereas there was a significant difference from the two small bees (p < 0.01, Steel-Dwass test). More over, the proportion of pollen and nectar foragers varied among bee species (Fig. 2). The proportion of O. orientalis that collected pollen was significantly higher than that of the two honeybees (p < 0.001, Fishers exact probability test). The pro portion of pollen foragers, i.e. both pollen-only and pollen-nectar foragers, for European honeybee and Japanese honeybees was 9.3 and 10.0% respectively, whereas for O. orientalis it was 52.1%. The proportion of individuals of Micrandrena spp. that collected pollen was significently different from that of the two honeybees (A. mellifera; p = , A. c. japonica; p = , Fishers exact probability test), whereas there was no difference from that of O. orientalis and C. flavipes. The proportion of individuals of C. flavipes that collected pollen was not significently different from the other four bees. The results of the present study showed that the foraging activity of the solitary bee O. orientalis is as high as that of both honeybee species. Moreover, O. orientalis might be an effective pollinator for wild raspberry because approximately 50% of O. orientalis individuals collected pollen, whereas 80% of visit-
5 Volume 125, Number 5, March ed individuals of two honeybees collected only nectar. A large proportion of the other solitary bees, C. flavipes and Micrandrena spp., also collected pollen. We suggest that in wild raspberry, the pollination efficiency of solitary bees might be higher than that of social bees. A comparison of the seed set rate or pollen transfer is required to evaluate true pollination efficacy. ACKNOWLEDGMENTS We owe great thanks to the members of the Laboratory of Entomology, Kindai University for collecting field data. This work was supported in part by the Program to Disseminate Tenure Tracking System, MEXT, Japan. LITERATURE CITED Bosch, J. and M. Blas Foraging behavior and pollinating efficiency of Osmia cornuta and Apis mellifera on almond (Hymenoptera, Megachilidae and Apidae). Applied Entomology and Zoology 29: 1-9. Cane, J. H Pollination potential of the bee Osmia aglaia for cultivated red raspberries and blackberries (Rubus: Rosaceae). HortScience 40: Maeta, Y Comparative studies on the biology of the bees of the genus Osmia of Japan, with special reference to their management for pollination of crops (Hymenoptera: Megachilidae). Bulletin of Tohoku National Agricultural Experimental Station 57: (In Japanese with Eng - lish summary.) Maeta, Y. and T. Kitamura Pollination efficiency by Osmia cornifrons in relation to re - quired number of nesting bees for economic fruit production. Honeybee Science 2: (In Jap - a nese.) Maeta, Y. and R. Miyanaga Distributional records of the seven species of genus Osmia in Japan (Hymenoptera, Megachilidae). Bulletin of Hoshizaki Green Foundation 3: (In Jap a nese.) Miyamoto, S. 1959a. Biological studies on Japanese bees VIII. Relationship between bees and flowers (Part 1). Japanese Journal of Ecology 9: (In Japanese with English summary.) Miyamoto, S. 1959b. Biological studies on Japanese bees IX. Relationship between bees and flowers (Part 2). Japanese Journal of Ecology 9: (In Japanese with English summary.) Monzón, V. H., J. Bosch, and J. Retana. (2004) Foraging behavior and pollinating effectiveness of Osmia cornuta (Hymenoptera: Megachilidae) and Apis mellifera (Hymenoptera: Apidae) on Comice pear. Apidologie 35: Rice, W. R Analyzing tables of statistical tests. Evolution 43: Sampson, B. J. and J. H. Cane Pollination efficiencies of three bee (Hymenoptera: Apoidea) species visiting rabbiteye blueberry. Journal of Economic Entomology 93: SAS Institute JMP release 11. Cary, NC: SAS Institute Inc. Vicens, N. and J. Bosch Pollinating efficacy of Osmia cornuta and Apis mellifera (Hymen- optera: Megachilidae, Apidae) on red delicious apple. Environmental Entomology 29:
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