About this Journal Submit a Manuscript Table of Contents
Volume 2010 (2010), Article ID 891906, 8 pages
Research Article

Flower Constancy in the Generalist Pollinator Ceratina flavipes (Hymenoptera: Apidae): An Evaluation by Pollen Analysis

1Faculty of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe 657-8501, Japan
2Graduate School of Environmental Science, Faculty of Environmental Earth Science, Hokkaido University, N10W5, Sapporo 060-0810, Hokkaido, Japan

Received 25 July 2009; Accepted 11 December 2009

Academic Editor: Claus Rasmussen

Copyright © 2010 Midori Kobayashi-Kidokoro and Seigo Higashi. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


The food habits of the solitary bee Ceratina flavipes were studied by observation on foraging behavior and identifying the pollen grains that they collected. It appeared that C. flavipes tend to collect pollen from particular species; however, they visit multiple flowering species. We analyzed pollen sources from pollen loads of dried specimens from single foraging trips (SFT) and in pollen balls created from a single foraging day (SD). The pollen from all pollen balls in a nest represented the harvest from an entire breeding season (BP). This analysis showed that each bee on average collected pollen from 3.24 (SFTs), 2.02 (SD), and 3.12 (BP) flowering species. Bees collected pollen from a total of 14 flowering plant species. Furthermore, we calculated when pollen balls were created and found no significant interaction between seasonal pollen availability and bee preferences. Moreover, bees had consistent flower preferences, even if the preferred flower was not dominant at all times. These results indicate that C. flavipes exhibits flower constancy, and therefore, the generalist pollinator C. flavipes could function like a specialist pollinator.

1. Introduction

Flower constancy means that a bee restricts its foraging activity to one or a few flowering species, even when many other flowers are available. Since the last century, flower constancy has been studied in honey bees [16], bumble bees [710], and a few other bee species [1113]. Flower constancy is an important behavior because it can enhance pollination efficiency for the plant and foraging efficiency for the pollinator. In eusocial bees, enhanced foraging efficiency by individual workers improves the colony survival rate. Thus, flower constancy has been studied extensively in eusocial bees [2, 10, 11].

The mechanisms of flower constancy in bees have been studied empirically [14, 15] and theoretically [16, 17], but are still unknown. Cognitive ability, vision [10], olfaction [6, 8], and memory [3, 5, 18] are thought to influence flower constancy. In solitary bees, foraging efficiency is also likely important; their olfactory sense is highly developed. For example, the solitary bee Lasioglossum figueresi uses odor to recognize the nest [19]. Thus, solitary bees may also have flower constancy. Pollen balls provided for offspring by solitary bees have been examined in Lasioglossum [19], Megachile [12], Heriades [12], and Osmia [13]; most pollen balls of these species contain pollen from only two to three plant species, suggesting flower constancy in the preparation of the pollen ball. In these solitary bee species only the plant species used for pollen balls can be noted because no data on the available flowers were provided.

Previous studies of flower constancy in eusocial bee species did not examine temporal variation in flower constancy throughout the breeding period because many were laboratory-based studies. It is difficult to follow bees individually or to identify offspring age in the field, making laboratory studies advantageous. However, flower resources in the field might influence foraging behavior.

Therefore, we explored the relationship between the availability of flower resources and flower constancy in the solitary, generalist pollinator bee Ceratina flavipes. The life history of C. flavipes has been well studied in Japan [2022]. We analyzed flower constancy based on pollen samples at three levels: a single foraging trip, a single day of foraging, and the entire breeding period. We defined flower constancy as when individual C. flavipes forages on fewer flowering species than the total number of plants used by all examined individuals of C. flavipes during the study.

2. Methods

2.1. Species and Study Site

Ceratina flavipes is the dominant species at the study site on the Ishikari Coast, Japan [23]. On the Ishikari Coast, a windbreak chaparral runs parallel to the shoreline, which is covered by a 200–300 m wide grassland vegetated by various wild flowering plants. Each female of C. flavipes digs a nest burrow in the stem of a dead grass shoot and oviposits several eggs during the breeding season. During the breeding season, females forage for pollen and nectar several times each day when weather conditions are suitable. Females make a pollen ball and lay an egg on it; the larva eats the pollen ball and grows within the cell. Generally, the female stores a pollen ball and an egg at each cell. The pollen balls and eggs are placed individually and in temporal order along the nest burrow. This behavior is advantageous because we can determine the order in which the eggs were laid. The breeding season of C. flavipes is from early June to late July in this study site.

The study site had about 22 flowering species, eight of which were observed in this study: Calystegia soldanella (Convolvulaceae), Lathyrus japonicus (Leguminosae), Melilotus suaveolens (Leguminosae), Oenothera biennis (Onagraceae), Picris hieracioides v. glabrescens (Compositae), Rosa parvifolius (Rosaceae), Rosa rugosa (Rosaceae), and Vicia cracca (Leguminosae). To study pollen resources used by C. flavipes, we placed 69 bee nests in the middle of a quadrate in the end of May 2000, before the bees started to oviposit. Set nests were collected from an area surrounding the study site.

2.2. Observation of Flower Visitation

A total of 13 nest-building female C. flavipes were followed and their foraging behavior observed from 8:00 to 14:00 on 18 and 20 June and 6, 7, and 11 July 2000. We observed marked bees as long as we could track them by eyes during observation periods (8:00–14:00). We then recorded (1) the flower species visited, (2) whether the individual moved between flowers within a plant, and (3) the behavior on the flower, which was classified into landing on the flower petals, staying on the central of flower without foraging pollen, and pollen foraging. For tracking observation, bees were caught and marked with paint marker at their abdomen. Each bee was marked with small dots of two colors and was identified by color combinations.

2.3. Pollen Analysis

We regarded the pollen load at the scopae of hind legs as the mean amount of pollen collected in a single trip. We regarded one pollen ball and all pollen balls in a nest as the mean amount of pollen collected in a single day and throughout a breeding season, respectively.

For the analysis of pollen collected in a single foraging trip, we used pollen attached to the scopae of 84 mounted specimens of bees sampled from several sites near the Ishikari Coast site in the past 10 years. These mounted specimens were caught at sites with more than two flowering plant species. Thus, we assumed that they had the opportunity to visit multiple plant species. To determine flower constancy within a single foraging trip, we used pollen loads from the pollen baskets of bee specimens that had been sampled at and near the study site within the last 10 years. We used dead specimens because collecting pollen loads from bees on each foraging trip would cause too much disturbance of the bee behavior.

For pollen collected in a single day or throughout the breeding period, we sampled 69 nests at the study site on 1 July 2000. We analyzed 253 pollen balls from these nests. When a pollen ball was already consumed by a larva, we collected the pollen ball particles and larval or pupal waste remaining in the cell.

We processed the pollen using the standard acetolysis method [24]. Pollen grains ( 𝑛 = 200) were randomly chosen from each sample and identified to species under a microscope, referring to technical pollen books [25, 26] and pollinic preparations. The pollinic preparations were samples of untreated pollen collected from flowers at the study site.

2.4. Estimation of Oviposition Date

Ceratina flavipes sequentially oviposits from the bottom upward in the nest. This behavior was used to estimate oviposition dates and the dates on which pollen balls were made. We divided the immature individuals into stages, and the developmental periods were allocated among the stages. Three larval stages were defined: “small larvae” whose legs were hard to identify (4 or 5 days after oviposition), “medium larvae” whose legs were easy to identify (11 to 13 days), and “large larvae” without a pollen ball (18 or 19 days). Eggs hatched within 1 or 2 days. Small larvae became medium larvae after 2 or 3 days. We used these developmental stages to back-calculate the oviposition dates of immature bees sampled from the set nests. We confirmed that the order of immatures in the nest and the pollen with each immature did not conflict with the phenological calendar. We recorded offspring stage (e.g., adult, pupa, larva, or egg) in order from the bottom of each nest. To determine the developmental period of each stage, we sampled 10 wild nests with immatures at the study site. After dissecting the 10 nests, each individual was placed in a vial with a pollen ball, kept at room temperature without air conditioning, and reared in the laboratory. For the hatching period, we selected the oldest and youngest eggs in the nest because we did not know when the eggs had been oviposited.

2.5. Available Pollen Resources and Flower Constancy

The availability of pollen resources in the field was compared with the pollen in the nests of individual bees from the pollen analysis. The availability was estimated by regularly counting the number of flowers and determining the average dry weight of pollen per flower in each focal species. We counted the number of open flowers of the eight focal species, treating the spicate of C. soldanella as one flower, within a 50 × 100 m quadrate once per week during the observation period (12 June to 1 July 2000). We also recorded the date of first flowering in each species. To calculate the average amount of pollen provided by a single flower per day, we selected several intact flower buds from each focal species at the edge of the study site (10 to 35 buds per species) and covered each bud with a small bag (3 × 4 cm) of fine mesh cloth. We collected five covered flowers every day from the start of flowering until petals dropped. Sampled flower heads were dried at room temperature, and the pollen was separated from other parts (i.e., anthers and petals) using a 1 mm wire mesh filter. The pollen was then completely dried in an incubator at 4 0 C for more than 1 week and weighed on an electronic balance.

3. Results

3.1. Flower Visitation

We successfully followed 13 marked bees and observed their flower visits (Figure 1). Although six bees visited two species, all C. flavipes individuals foraged exclusively for pollen on a particular species, except bee number 5 that collected pollen from two plant species.

Figure 1: Consecutive visits to flowers by marked Ceratina flavipes in late June 2000 at the study quadrat. Ishikari study site. Each alphabet indicate flowering species, A: Rosa rugosa; B: Rosa parvifolius; C: Picris hieracioides v. glabrescens; D: Lathyrus japonicus; E: Calystegia soldanella. And each marks indicated the behaviors, =: Moving within same stem; -: Moving to another stem. Bord face letter indicates collection of pollen, underline indicates staying at central of flower witout collecting pollen, and standard face letter indicates landing on the flower petals.
3.2. Pollen Analysis

The 14 plant species found in the pollen analysis included the eight focal species. The mean (maximum in parenthesis) number of plant species was 3.24 (7), 2.02 (5), and 3.12 (6) for pollen collected in a single foraging trip (SFT), a single day (SD), and the breeding period (BP), respectively (Table 1). We found that the mean number of plant species visited was relatively low, with 55 (SFT), 227 (SD), and 50 (BP) of pollen load composed by more than 80% of same species, furthermore, some of them, 6 (SFT), 94 (SD), and 9 (BP), composed by 100% of same species within analyzed 200 pollen grants (Table 1). These results indicate that C. flavipes shows flower constancy, although it is a generalist pollinator. Flower constancy means that an individual visits some flowering species regularly, although, overall, different individuals of C. flavipes visit various flowering species to obtain resources.

Table 1: Composition of pollen grains ( 𝑛 = 200) randomly chosen from each of 84 pollen loads and 253 pollen balls.
3.3. Oviposition Date

Of the immature bees that we reared from 10 nests sampled in the field, 39 were female and 31 were male. Eggs and small, medium, and large larvae were oviposited on 30 June or 1 July; 26 or 27 June; 18, 19, or 20 June; and 12 or 13 June, respectively (Figure 2(b)). These results coincide with the pollen analysis and the phenology of the eightfocal plant species at the study site (Table 2, Figure 2(a)).

Table 2: Species of pollen grains contained in cells for each developmental stage collected on 1 July. + : present; : absent; LL: large larva; ML: medium larva; SL: small larva; E: egg. Sum of set 69 nests and sampled 10 nests for determination of developmental period, was shown in this table.
Figure 2: (a) Flowering phenology on the Isikakri Coast and (b) oviposition dates (i.e., dates when pollen balls were made) inferred from the rearing of immature individuals in the laboratory. Nests with pollen balls, eggs, larvae, pupae, and adults were sampled on 1 July. The thick line in (a) represents the starting dates of the flowering period of each flowering species at the field. The date axis in (a) is common with in (b).
3.4. Available Pollen Resources and Flower Constancy

The pollen availability of each species was estimated as the product of the dry weight of pollen per flower head and the number of flowers (Table 3). The mean dry weight of pollen per flower decreased in the following order: V. cracca, R. rugosa, R. parvifolius, M. suaveolens, P. hieracioides v. glabrescens, L. japonicus, O. biennis, and C. soldanella. There was interspecific variation in the flowering period; the longest was that of M. suaveolens and the shortest was that of C. soldanella (Table 3). Pollen availability was not significantly related to bee flower preference at any developmental stage (Table 4; 𝐺 -tests, egg: 𝑋 2 = 9979.381, 𝑃 < . 0 1 ; small larvae: 𝑋 2 = 11782.85, 𝑃 < . 0 1 ; medium larvae: 𝑋 2 = 22632.59, 𝑃 < . 0 1 ; large larvae: 𝑋 2 = 24017.79, 𝑃 < .01).

Table 3: Weight (mg) of desiccated pollen per flower head on each day after the initiation of flowering (see Figure 2(a) for each species). Mean ± standard deviation of five flower heads. Average pollen production (P) was used to calculate pollen availability within a 50 × 100 m quadrat (cf. Table 4). Names of flowering species are arranged in descending order average pollen production.
Table 4: Comparison of pollen availability and pollen usage by Ceratina flavipes and Phenology of the total dry weight of pollen for each flowering species during the breeding season of C. flavipes. The number of flowers is shown in parentheses. Total pollen mass was calculated as 𝑚 × 𝑛 , where m is the average dry pollen weight per flower (from Table 3) and 𝑛 is the number of flowers. Availability and usage differed significantly among species.

In nine nests, all pollen balls in the nest were composed of a single plant species, that is, R. rugosa or R. parvifolius. Although R. parvifolius was not a dominant species at the beginning of the breeding season, three female bees constantly foraged on R. parvifolius.

4. Discussion

Flower gardens in temperate areas can be beautiful, because various species flower in a short period of time. In this study site, which was located in a cool-temperate area, 22 plant species flowered concurrently. There was interspecific variation in flower density with R. parvifolius being one of the rarest. Although a rare species might require a specialized pollinator, we did not observe specialist pollinators on 1 July. However, generalist pollinators can also function as specialized pollinators if they exhibit flower constancy. C. flavipes showed flower constancy in its pollen foraging (Table 1), and the intensity of its flower constancy seemed to vary intraspecifically.

We studied flower constancy of polylectic solitary bee, C. flavipes with observation of foraging behavior for SFT, pollen analysis from pollen attached specimens for SD, and that from pollen ball in the nest for BP. It is difficult to conclude with each result from SFT, SD, and BP, because there are some limitations due to the small number of foraging observations (SFT), uncertainty of foraging information of specimens (SD), and lack of uniformity in estimation of flower availability (BP). However, these limitation needs to be dealt with in a separate studies, considering all the results together in this study, it is possible to regard C. flavipes to have flower constancy.

Ceratina flavipes tended to prefer certain plant species (Figure 1), these data are insufficient because observations were made were not tested experimentally. Our results, however, indicate a preference of C. flavipes for R. rugosa and R. parvifolius pollen at this study site (Table 4). Other flowering species were uncommon in pollen balls, although the availability of some species was high (Table 4). The uncommon species in pollen balls may result from bee behavior, such as casual landing or nectar feeding. Although the individual bees exhibited flower constancy, many flowering species were used (Figure 1). Thus, the percentage of pollen grains represented by the most dominant plant species was low (Table 1), indicating that bees may choose to collect pollen from a particular flowering species.

The mechanisms and causes of flower constancy in pollinators still remain elusive. Many conceptual and empirical studies suggest that the cognitive and memorization abilities of pollinators are important determinants of flower constancy. In theoretical studies, based on a classical patch model [27], optimal strategies with an important parameter, that is, individual memory, have been constructed [16, 17]. Bees have the cognitive ability to recognize floral colors [10, 28]; furthermore, the cognitive ability to recognize odors has been explored, especially in bumble bees [7, 8] and honeybees [36]. The memory of an individual forager is the primary contributor to flower constancy [18]. Previous studies have suggested that generalist pollinators are effective pollinators for angiosperms [2931]. Flower constancy increases the effectiveness of pollination by generalist pollinators [32]. The various determinants of flower constancy are connected via neural substrates [33]. These factors are regulated by the highly developed sensory systems in the bees [4, 34, 35].

Flower traits (i.e., odor, color, and shape) might motivate bees to select certain flowers when foraging. In particular, olfactory sensations might be important, particularly for bees, because olfaction is used to find particular plant species [5, 6, 8] and to recognize the nest [19]. However, bees’ ability to remember flower traits is limited; it is unclear how many flower traits bees can memorize and/or discriminate among when foraging. To determine the mechanisms of flower constancy in bees, the relationship between memorization and learning of particular plant species and the foraging behavior of the bees must be determined.

Although the lifecycles of some bee species are known, the timing of memorization and learning remain unclear. In C. flavipes, prior studies describing the life cycle indicate that individuals have opportunities to memorize pollen species at different developmental stages: when growing on a pollen ball provided by the mother, when they eclose with frass in the cell, when they are provided with nectar and pollen by their mother or elder sisters after the breeding season, when they first forage by themselves during dispersal in the prehibernation season, or when they start foraging by themselves at the beginning of the nesting and/or breeding season after hibernation[23, 3639]. Holometabolous insects have different nervous systems as adults than they do as juveniles [40]; thus, memories acquired as a juvenile may be lost during metamorphosis. Combined with the results of prior studies, our results suggest that the memorization required for flower constancy is more likely to occur in the prehibernation season, that is, the period from emergence to hibernation, than in other stages.

Our quadrate was near the maximum size in this study area, but there are some small vegetation patches around the study area, such as parking areas. The V. cracca, R. parvifolius, and P. hieracioides pollen were found from pollen balls; however, we did not observe these plant species at the study area during the putative period (6/12-13) (Table 4). The results suggested that the bee might forage beyond our study quadrate to seek for the particular flowering species. Furthermore, a species might be memorized before hibernation, the first foraging period of C. flavipes, as the olfactory information acquired in the early days after emergence modifies bees' later behavior in honeybee [18].

These facts together suggest that the foraging behavior of adults is determined by adult experiences in the prehibernation season. However, this may not always be the case. C. flavipes is also found in temperate areas, where it is unlikely that bees use information memorized before hibernation because the flowering species are completely different at the beginning and ending of the breeding period. In addition, many solitary generalist bees eclose only after hibernation [12, 19, 4143]. To determine the mechanisms of flower constancy in solitary, social, and generalist bees, the relationships between learning, memorization, and forging behavior should be examined using behavioral observations and neurobiological methods.


The authors thank M. Fukuda (Hokkaido University) for help with the study of C. flavipes, N. Hagihara for technical support with the pollen analysis, S. Sakai and Y. Kobayashi (CER Kyoto University) for helpful advice on the manuscript, and colleagues in the Higashi laboratory at the Hokkaido University, for useful discussion.


  1. B. Heinrich, “Energetics of pollination,” Annual Review of Ecology and Systematics, vol. 6, pp. 139–170, 1975. View at Google Scholar
  2. H. Wells and P. H. Wells, “Honey bee foraging ecology: optimal diet, minimal uncertainty or individual constancy?” Journal of Animal Ecology, vol. 52, no. 3, pp. 829–836, 1983. View at Google Scholar
  3. R. S. Thorn and B. H. Smith, “The olfactory memory of the honeybee Apis Mellifera. III. Bilateral sensory input is necessary for induction and expression of olfactory blocking,” Journal of Experimental Biology, vol. 200, no. 14, pp. 2045–2055, 1997. View at Google Scholar
  4. B. Gerber and B. H. Smith, “Visual modulation of olfactory learning in honey bees,” Journal of Experimental Biology, vol. 201, pp. 2213–2217, 1998. View at Google Scholar
  5. D. Laloi, B. Roger, M. M. Blight, L. J. Wadhams, and M.-H. Pham-Delègue, “Individual learning ability and complex odor recognition in the honey bee, Apis mellifera L,” Journal of Insect Behavior, vol. 12, no. 5, pp. 585–597, 1999. View at Google Scholar
  6. S. M. Cook, J.-C. Sandoz, A. P. Martin, D. A. Murray, G. M. Poppy, and I. H. Williams, “Could learning of pollen odours by honey bees (Apis mellifera) play a role in their foraging behaviour?” Physiological Entomology, vol. 30, no. 2, pp. 164–174, 2005. View at Publisher · View at Google Scholar
  7. L. Chittka and J. D. Thomson, “Sensori-motor learning and its relevance for task specialization in bumble bees,” Behavioral Ecology and Sociobiology, vol. 41, no. 6, pp. 385–398, 1997. View at Publisher · View at Google Scholar
  8. D. Laloi, J. C. Sandoz, A. L. Picard-Nizou, et al., “Olfactory conditioning of the proboscis extension in bumble bees,” Entomologia Experimentalis et Applicata, vol. 90, no. 2, pp. 123–129, 1999. View at Publisher · View at Google Scholar
  9. D. Goulson, “Are insects flower constant because they use search images to find flowers?” Oikos, vol. 88, no. 3, pp. 547–552, 2000. View at Google Scholar
  10. R. J. Gegear and T. M. Laverty, “Flower constancy in bumblebees: a test of the trait variability hypothesis,” Animal Behaviour, vol. 69, no. 4, pp. 939–949, 2005. View at Publisher · View at Google Scholar
  11. D. White, B. W. Cribb, and T. A. Heard, “Flower constancy of the stingless bee Trigona carbonaria Smith (Hymenoptera: Apidae: Meliponini),” Australian Journal of Entomology, vol. 40, no. 1, pp. 61–64, 2001. View at Publisher · View at Google Scholar
  12. P. D. Jensen, K. M. O'Neill, and M. Lavin, “Pollen provision records for three solitary bee species of Megachile Latreille and Heriades Spinola (Hymenoptera: Megachilidae) in southwestern Montana,” Proceedings of the Entomological Society of Washington, vol. 105, no. 1, pp. 195–202, 2003. View at Google Scholar
  13. S. Matsumoto, A. Abe, and T. Maejima, “Foraging behavior of Osmia cornifrons in an apple orchard,” Scientia Horticulturae, vol. 121, no. 1, pp. 73–79, 2009. View at Publisher · View at Google Scholar
  14. N. M. Waser, “Flower constancy: definition, cause, and measurements,” American Naturalist, vol. 127, pp. 593–603, 1986. View at Google Scholar
  15. G. L. Woodward and T. M. Laverty, “Recall of flower handling skills by bumble bees: a test of Darwin's interference hypothesis,” Animal Behaviour, vol. 44, no. 6, pp. 1045–1051, 1992. View at Google Scholar
  16. K. Ohashi and T. Yahara, “How long to stay on, and how often to visit a flowering plant? A model for foraging strategy when floral displays vary in size,” Oikos, vol. 86, no. 2, pp. 386–391, 1999. View at Google Scholar
  17. K. Ohashi and T. Yahara, “Visit larger displays but probe proportionally fewer flowers: counterintuitive behaviour of nectar-collecting bumble bees achieves an ideal free distribution,” Functional Ecology, vol. 16, no. 4, pp. 492–503, 2002. View at Publisher · View at Google Scholar
  18. J. C. Sandoz, D. Laloi, J. F. Odoux, and M.-H. Pham-Delègue, “Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure,” Animal Behaviour, vol. 59, no. 5, pp. 1025–1034, 2000. View at Publisher · View at Google Scholar · View at PubMed
  19. W. T. Wcislo, “Nest localization and recognition in a solitary bee, Lasioglossum (Dialictus) figueresi Wcislo (Hymenoptera: Halictidae), in relation to sociality,” Ethology, vol. 92, pp. 108–123, 1992. View at Google Scholar
  20. S. F. Sakagami and Y. Maeta, “Sociality, induced and/or natural, in the basically solitary small carpenter bees (Ceratina),” in Animal Societies: Theories and Facts, Scientific Society, Tokyo, Japan, 1987. View at Google Scholar
  21. Y. Maeta, E. S. de la Asensio, and S. F. Sakagami, “Comparative studies on the in-nest behaviors of small carpenter bees, the genus Ceratina (Hymenoptera, Anthophoridae, Xylocopinae). I. Ceratina (Ceratina) cucurbitina—part 1,” Japanese Journal of Entomology, vol. 65, pp. 303–319, 1997. View at Google Scholar
  22. Y. Maeta, E. S. de la Asensio, and S. F. Sakagami, “Comparative studies on the in-nest behaviors of small carpenter bees, the genus Ceratina (Hymenoptera, Anthophoridae, Xylocopinae). I. Ceratina (Ceratina) cucurbitina—part 2,” Japanese Journal of Entomology, vol. 65, pp. 471–481, 1997. View at Google Scholar
  23. M. Kidokoro, T. Kikuchi, and M. Hirata, “Prehibernal insemination and short dispersal of Ceratina flavipes (Hymenoptera: Anthophidae) in northernmost Japan,” Ecological Research, vol. 18, no. 1, pp. 99–102, 2003. View at Publisher · View at Google Scholar
  24. A. C. Kearns and D. W. Inouye, Techniques for Pollination Biologists, University of Colorado, Boulder, Colo, USA, 1993.
  25. J. Nakamura, Diagnostic Characters of Pollen Grains of Japan, Part 1, vol. 12, Special Publications from the Osaka Museum of Natural History, Osaka, Japan, 1980.
  26. J. Nakamura, Diagnostic Characters of Pollen Grains of Japan, Part 2, vol. 13, Special Publications from the Osaka Museum of Natural History, Osaka, Japan, 1980.
  27. E. L. Charnov, “Optimal foraging, the marginal value theorem,” Theoretical Population Biology, vol. 9, no. 2, pp. 129–136, 1976. View at Google Scholar
  28. T. C. Ings, N. E. Raine, and L. Chittka, “A population comparison of the strength and persistence of innate colour preference and learning speed in the bumblebee Bombus terrestris,” Behavioral Ecology and Sociobiology, vol. 63, no. 8, pp. 1207–1218, 2009. View at Publisher · View at Google Scholar
  29. F. Gilbert, S. Azmeh, C. Barnard, et al., “Individually recognizable scent marks on flowers made by a solitary bee,” Animal Behaviour, vol. 61, no. 1, pp. 217–229, 2001. View at Publisher · View at Google Scholar · View at PubMed
  30. S. G. Potts, A. Dafni, and G. Ne'Eman, “Pollination of a core flowering shrub species in Mediterranean phrygana: variation in pollinator diversity, abundance and effectiveness in response to fire,” Oikos, vol. 92, no. 1, pp. 71–80, 2001. View at Google Scholar
  31. I. Steffan-Dewenter, U. Münzenberg, C. Bürger, C. Thies, and T. Tscharntke, “Scale-dependent effects of landscape context on three pollinator guilds,” Ecology, vol. 83, no. 5, pp. 1421–1432, 2002. View at Google Scholar
  32. L. Chittka, J. D. Thomson, and N. M. Waser, “Flower constancy, insect psychology, and plant evolution,” Naturwissenschaften, vol. 86, no. 8, pp. 361–377, 1999. View at Publisher · View at Google Scholar
  33. R. Menzel, “Searching for the memory trace in a mini-brain, the honeybee,” Learning and Memory, vol. 8, no. 2, pp. 53–62, 2001. View at Publisher · View at Google Scholar · View at PubMed
  34. S. Andersson, “Floral display and pollination success in Senecio jacobaea (Asteraceae): interactive effects of head and corymb size,” American Journal of Botany, vol. 83, no. 1, pp. 71–75, 1996. View at Google Scholar
  35. P. Wilson, M. C. Castellanos, J. N. Hogue, J. D. Thomson, and W. S. Armbruster, “A multivariate search for pollination syndromes among penstemons,” Oikos, vol. 104, no. 2, pp. 345–361, 2004. View at Publisher · View at Google Scholar
  36. S. F. Sakagami, “Multi-female nests and rudimentary castes of an “almost” solitary bee Ceratina flavipes, with additional observations on multi-female nests of Ceratina japonica (Hymenoptera, Apodiea),” Kontyu Tokyo, vol. 55, pp. 391–409, 1987. View at Google Scholar
  37. Y. Maeta, N. Sugiura, and M. Goubara, “Patterns of offspring production and sex allocation in the small carpenter bee, Ceratina flavipes Smith (Hymenoptera, Xylocopinae),” Japanese Journal of Entomology, vol. 60, pp. 175–190, 1992. View at Google Scholar
  38. Y. Maeta, K. Saito, K. Hyodo, and S. F. Sakagami, “Diapause and non-delayed eusociality in a univoltine and basically solitary bee, Ceratina japonica (Hymenoptera, Anthophoridae). I. Diapause termination by cooling and application of juvenile hormone analog,” Japanese Journal of Entomology, vol. 61, pp. 203–211, 1993. View at Google Scholar
  39. S. F. Sakagami and Y. Maeta, “Task allocation in artificially induced colonies of a basically solitary bee Ceratina (Ceratinidia) okinawana, with a comparison of sociality between Ceratina and Xylocopa (Hymenoptera, Anthophoridae, Xylocopinae),” Japanese Journal of Entomology, vol. 63, pp. 115–150, 1995. View at Google Scholar
  40. J. W. Truman, “The eclosion hormone system of insects,” Progress in Brain Research, vol. 92, pp. 361–374, 1992. View at Google Scholar
  41. M. L. Peach, D. G. Alston, and V. J. Tepedio, “Sublethal effects of carbaryl bran bait on nesting performance, parental investment, and offspring size and sex ratio of the alfalfa leafcutting bee (Hymenoptera: Megachilidae),” Environmental Entomology, vol. 24, pp. 34–39, 1995. View at Google Scholar
  42. K. Hogendoorn, N. L. Watiniasih, and M. P. Schwarz, “Extended alloparental care in the almost solitary bee Exoneurella eremophila (Hymenoptera: Apidae),” Behavioral Ecology and Sociobiology, vol. 50, no. 3, pp. 275–282, 2001. View at Publisher · View at Google Scholar
  43. J. Bosch and N. Vicens, “Body size as an estimator of production costs in a solitary bee,” Ecological Entomology, vol. 27, no. 2, pp. 129–137, 2002. View at Publisher · View at Google Scholar