Assessing the impact of the invasive buff-tailed bumblebee (Bombus terrestris) on the pollination of the native Chilean herb Mimulus luteus

The arrival of exotic pollinators to new habitats may introduce new patterns of floral preference and foraging behavior that modify the structure of the resident plant–pollinator community. The aim of this paper is to examine the potential impact of the exotic bumblebee Bombus terrestris on the pollination service provided by the native pollinator assemblage of the herb Mimulus luteus. The study was performed in a high-elevation locality in the Chilean Andes during the summer seasons of 2010, 2011, and 2012. We recorded visitation rate, and the number of pollen grains transported on the body of B. terrestris and native pollinators and the pollen deposition on the stigmas of M. luteus. Pollinator effectiveness (pollen deposited × visitation rate) was compared among species. Results revealed that B. terrestris was an inefficient pollinator, due to the low amount of pollen delivered on stigmas and the low and intermittent visitation rate across years. The parallel inter-annual variation in the visitation rate of B. terrestris and the native bumblebee Bombus dahlbomii suggests that the integration of B. terrestris had no important consequences for the congeneric species. In general, B. terrestris accounted for a low proportion of the pollen transfer in M. luteus, reaching 4.6 % in 2010, absence of effect in 2011, and 0.01 % in 2012. These results suggest that in spite of being a quickly spreading species in Chile, B. terrestris is still in the initial phase of invasion in this area.     

The bumblebee Bombus ardens ardens (Hymenoptera: Apidae) visits white clover in orchards before Oriental persimmon blooms

Flowers on the ground of orchards can provide substantial resources for wild pollinators of orchard trees. Few studies, however, have examined the relative importance of groundcover flowers to orchard pollination by analyzing pollen on the body surface of pollinators. Oriental persimmon trees bloom within the longer blooming period of white clover, which is occasionally found as a flowering plant on the ground of persimmon orchards in Japan. The present study compared the insect species assemblage collected on persimmon flowers with that on clover. Before persimmon bloomed, Bombus ardens ardens and Apis cerana japonica were the major visitors of clover flowers. Once persimmon bloomed, the former was the most abundant bee that visited persimmon flowers over the flowering period. Apis mellifera was captured only on clover flowers. We found numerous clover pollen grains on the body surface of bumblebees captured on persimmon flowers, but far fewer persimmon pollen grains on bees that visited clover. These findings show that B. ardens ardens utilized the clover flowers under the orchards before persimmon bloomed.     

Variation in composition of two bumble bee species across communities affects nectar robbing but maintains pollinator visitation rate to an alpine plant,Salvia przewalskii

1. In many flowering plants, bumble bees may forage as both pollinators and nectar robbers. This mixed foraging behaviour may be influenced by community context and consequently, potentially affect pollination of the focal plant. 2. Salvia przewalskii is both pollinated and robbed exclusively by bumble bees. In the present study area, it was legitimately visited by two species of bumble bees with different tongue length, Bombus friseanus and Bombus religiosus, but it was only robbed by Bombus friseanus, the shorter‐tongued bumble bee. The intensity of nectar robbing and pollinator visitation rate to the plant were investigated across 26 communities in the Hengduan Mountains in East Himalaya during a 2‐year project. For each of these communities, the floral diversity, and the population size and floral resource of S. przewalskii were quantified. The abundances of the two bumble bee species were also recorded. 3. Both nectar robbing and pollinator visitation rate were influenced by floral diversity. However, pollinator visitation rate was not affected by nectar robbing. The results revealed that relative abundance of the two bumble bee species significantly influenced the incidence of nectar robbing but not the pollinator visitation rate. Increased abundance of B. religiosus, the legitimate visitors, exacerbated nectar robbing, possibly by causing B. friseanus to shift to robbing; however, pollinator visitation remained at a relatively high level. 4. The results may help to explain the persistence of both nectar robbing and pollination, and suggest that, in comparison to pollination, nectar robbing is a more unstable event in a community.     

Minimal Effects of an Invasive Flowering Shrub on the Pollinator Community of Native Forbs

Biological invasions can strongly influence species interactions such as pollination. Most of the documented effects of exotic plant species on plant-pollinator interactions have been observational studies using single pairs of native and exotic plants, and have focused on dominant exotic plant species. We know little about how exotic plants alter interactions in entire communities of plants and pollinators, especially at low to medium invader densities. In this study, we began to address these gaps by experimentally removing the flowers of a showy invasive shrub, Rosa multiflora, and evaluating its effects on the frequency, richness, and composition of bee visitors to co-flowering native plants. We found that while R. multiflora increased plot-level richness of bee visitors to co-flowering native plant species at some sites, its presence had no significant effects on bee visitation rate, visitor richness, bee community composition, or abundance overall. In addition, we found that compared to co-flowering natives, R. multiflora was a generalist plant that primarily received visits from generalist bee species shared with native plant species. Our results suggest that exotic plants such as R. multiflora may facilitate native plant pollination in a community context by attracting a more diverse assemblage of pollinators, but have limited and idiosyncratic effects on the resident plant-pollinator network in general.     

So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort

Plant–pollinator interactions are one of the most important and variable mutualisms having major implications for plant fitness. The present study evaluates the interactions between an endemic milkwort, Polygala vayredae, and its floral visitors by studying the temporal variability, foraging behaviour and effectiveness of floral visitors in three populations during three consecutive years. The flowers were visited by a diverse array of insects, totalling 24 different species. However, only four species were effective pollinators, depositing pollen on stigmas after one visit, while the remaining species behaved as nectar robbers, secondary nectar robbers or nectar thieves and were completely ineffective for pollination. Among the effective pollinators, two groups with distinct foraging behaviours were observed: the nectar collecting long-tongued bees Bombus pascuorum and Anthophora sp. and the pollen collectors Eucera longicornis and Halictus sp. No significant differences were observed among pollinators in their efficiency in pollen deposition on stigmas, but significant differences were observed in the foraging behaviour between nectarivorous and pollen collectors. Variation in the abundance and assemblage of floral visitors was observed at the temporal scale and among populations, with the effective pollinators being generally scarce. Consequently, the reproductive outcome in this species was low and significantly variable among populations and years. The results highlight the importance of studying floral visitor effectiveness when determining pollinator assemblages.     

Temporal changes in calyx tube length of Clematis stans (Ranunculaceae): a strategy for pollination by two bumble bee species with different proboscis lengths

We examined the adaptive significance of a temporal decrease in the calyx tube length of Clematis stans, a dioecious species pollinated by Bombus diversus (long proboscis) and B. honshuensis (short proboscis). We compared visitation frequency, pollen removal, pollen deposition, and fruit set after a single visit among three flower stages, differentiated by calyx tube length. Bombus diversus frequently visited and removed significantly more pollen from long flowers. Bombus honshuensis visited and tended to remove more pollen from short flowers. Both pollinators deposited more pollen in short flowers, resulting in higher fruit set. These results indicate that size correspondence between the proboscis and the calyx tube enhances visitation frequency and pollen removal, but not pollen deposition. Because a single visit does not fertilize all ovules of a flower, multiple visits by two bumble bee species may increase seed production and genetic diversity of offspring. By temporally changing calyx tube length, C. stans can use two bumble bee pollinators and maintain specialized relationships with each. This strategy may be adaptive when the pollinator fauna fluctuates, and is economical because it eliminates costs required to produce different types of flowers. This constitutes a novel pattern of temporal specialization in flower-pollinator relationships.     

The role of individual variation in flowering and pollination in the reproductive success of a crepuscular buzz-pollinated plant

Background and AimsPlant individuals within a population differ in their phenology and interactions with pollinators. However, it is still unknown how individual differences affect the reproductive success of plants that have functionally specialized pollination systems. Here, we evaluated whether plant individual specialization in phenology (temporal specialization) and in pollination (pollinator specialization) affect the reproductive success of the crepuscular-bee-pollinated plant Trembleya laniflora (Melastomataceae).MethodsWe quantified flowering activity (amplitude, duration and overlap), plant–pollinator interactions (number of flowers visited by pollinators) and reproductive success (fruit set) of T. laniflora individuals from three distinct locations in rupestrian grasslands of southeastern Brazil. We estimated the degree of individual temporal specialization in flowering phenology and of individual specialization in plant–pollinator interactions, and tested their relationship with plant reproductive success.Key Results Trembleya laniflora presented overlapping flowering, a temporal generalization and specialized pollinator interactions. Flowering overlap among individuals and populations was higher than expected by chance but did not affect the individual interactions with pollinators and nor their reproductive success. In contrast, higher individual generalization in the interactions with pollinators was related to higher individual reproductive success.ConclusionsOur findings suggest that individual generalization in plant–pollinator interaction reduces the potential costs of specialization at the species level, ensuring reproductive success. Altogether, our results highlight the complexity of specialization/generalization of plant–pollinator interactions at distinct levels of organization, from individuals to populations, to species.     

Pollination ecology in sympatric winter flowering Helleborus (Ranunculaceae)

We studied biotic and abiotic factors that influence pollination in two sympatric winter flowering species. Helleborus foetidus and Helleborus bocconei flower simultaneously in winter. Although climatic conditions are not favorable for biotic pollination both species rely mainly on large bees of the genus Bombus. At the beginning of flowering, harsh climatic conditions are restrictive for insect visits. As flowering continues and temperatures rise, pollinator activity increases. The two plant species share pollinators that visit them indiscriminately. The flowers of the two species differ in form and insects visit H. foetidus by inserting their heads and H. bocconei ventrally: pollen load on insects is highly specialized. With the arrival of spring, many other species start to bloom and in spite of the large number of flowers still on the plants insects abandon Helleborus species. At the end of spring increasing biotic interactions take away pollinators from the Helleborus species.     

The reproductive biology of two understory plants in the Atlantic rain forest, Brazil

Outcrossing and sexual reproduction of most flowering plants depends on pollinators. Plant traits likely to be involved in pollinator attraction include flower color, shape, and size. Furthermore, plant or flower density and the temporal flowering pattern may have an effect on reproduction. In this study, we examine the pollination ecology, breeding system, female reproductive output, and germination of two tropical understory species, Stenostephanus lobeliiformis (Acanthaceae) and Besleria melancholica (Gesneriaceae), which differ in these traits. Pollinator observations revealed that the dense flowering S. lobeliiformis with pinkish flowers received a higher diversity of pollinators, but visitor frequency measured as visits per flower per hour was much less (0.1 h^?1) than that to B. melancholica, which has a smaller floral display of dull-colored flowers (1.5 h^?1). Pollination experiments revealed that S. lobeliiformis but not B. melancholica is pollen-limited. In addition, both species are partially self-incompatible and depend on pollinators for outcrossing. Natural fruit set of open-pollinated unmanipulated flowers (control treatment) in both species is 22–26 %. Germination studies indicated inbreeding depression in S. lobeliiformis. We conclude that the pollination ecology of these species is influenced by a broad set of traits and that very different combinations of these traits can be successful in terms of reproduction.     

The Abundance and Pollen Foraging Behaviour of Bumble Bees in Relation to Population Size of Whortleberry (Vaccinium uliginosum)

Habitat fragmentation can have severe effects on plant pollinator interactions, for example changing the foraging behaviour of pollinators. To date, the impact of plant population size on pollen collection by pollinators has not yet been investigated. From 2008 to 2010, we monitored nine bumble bee species (Bombus campestris, Bombus hortorum s.l., Bombus hypnorum, Bombus lapidarius, Bombus pascuorum, Bombus pratorum, Bombus soroensis, Bombus terrestris s.l., Bombus vestalis s.l.) on Vaccinium uliginosum (Ericaceae) in up to nine populations in Belgium ranging in size from 80 m² to over 3.1 ha. Bumble bee abundance declined with decreasing plant population size, and especially the proportion of individuals of large bumble bee species diminished in smaller populations. The most remarkable and novel observation was that bumble bees seemed to switch foraging behaviour according to population size: while they collected both pollen and nectar in large populations, they largely neglected pollen collection in small populations. This pattern was due to large bumble bee species, which seem thus to be more likely to suffer from pollen shortages in smaller habitat fragments. Comparing pollen loads of bumble bees we found that fidelity to V. uliginosum pollen did not depend on plant population size but rather on the extent shrub cover and/or openness of the site. Bumble bees collected pollen only from three plant species (V. uliginosum, Sorbus aucuparia and Cytisus scoparius). We also did not discover any pollination limitation of V. uliginosum in small populations. We conclude that habitat fragmentation might not immediately threaten the pollination of V. uliginosum, nevertheless, it provides important nectar and pollen resources for bumble bees and declining populations of this plant could have negative effects for its pollinators. The finding that large bumble bee species abandon pollen collection when plant populations become small is of interest when considering plant and bumble bee conservation.     

Plant traits and landscape simplification drive intraspecific trait diversity of Bombus terrestris in wildflower plantings

Wildflower plantings are an important mitigation tool within agri-environmental schemes to counter insect decline in resource-scarce agricultural landscapes. Effectiveness of wildflower plantings for insect conservation is typically studied at the community or species level. It is the individual, however, that is subject to changing abiotic and biotic conditions, not the species per se. Accordingly, functional traits of individuals, i.e., the intraspecific functional diversity within species, likely mediate responses to wildflower resources and landscape context. Here we focused on the ecologically and economically important wild insect pollinator Bombus terrestris to study its intraspecific functional diversity and plant-pollinator individual interactions in wildflower plantings. We found considerable trait variation among flower-visiting B. terrestris workers. Locally, this variation could be attributed to flowering plant traits, with larger workers visiting larger inflorescences and individuals with longer tongues preferentially feeding on zygomorphic but not radially symmetrical flowers. In addition, wildflower plantings with high floral abundance attracted individuals with larger pollen baskets. At the landscape scale, increasing proportion of arable land resulted in smaller B. terrestris individuals in wildflower plantings, and a decrease in the overall size diversity of workers. These findings highlight the so far little considered role of intraspecific variation in functional traits of wild pollinators, which can mediate the trait-matching between plants and pollinator individuals. Landscape simplification from agriculture threatens intraspecific pollinator diversity, with potential harmful effects for pollinator fitness and plant reproduction. Tailored wildflower plantings can thus serve as an important tool to increase intraspecific variation in simplified landscapes. When designing seed mixtures for these plantings, high complementarity in plant traits is key for promoting high intraspecific trait diversity of bumblebees and potentially of other associated insect species.     

Floral divergence and temporal pollinator partitioning in two synchronopatric species of <Emphasis Type="Italic">Vigna</Emphasis> (Leguminosae-Papilionoideae)

Exclusivity of pollinators, temporal partitioning of shared pollinators and divergence in pollen placement on the shared pollinators’ bodies are mechanisms that prevent interspecific pollen flow and minimize competitive interactions in synchronopatric plant species. We investigated the floral biology, flower visitors, pollinator effectiveness and seasonal flower availability of two syntopic legume species of the genus Vigna, V. longifolia and V. luteola, in ‘restinga’ vegetation of an island in southern Brazil. Our goal was to identify the strategies that might mitigate negative consequences of their synchronous flowering. Vigna longifolia and V. luteola were self-compatible, but depended on pollinators to set seeds. Only medium to large bees were able to trigger the ‘brush type’ pollination mechanism. Vigna longifolia, with its asymmetrical corolla and hugging mechanism, showed a more restrictive pollination system, with precise sites of pollen deposition/removal on the bee’s body, compared to V. luteola, with its zygomorphic corolla and cymbiform keel. There was a daily temporal substitution in flower visitation by the main pollinators. Vigna longifolia and V. luteola had overlapping flowering phenology but the densities of their flowers fluctuated, resulting in a seasonal partitioning of flower visitation. The differences in corolla symmetry and mainly the temporal partitioning among pollinators throughout the day and the flowering season proved to be important factors in maintaining the synchronopatry of V. longifolia and V. luteola.     

Increase in ant density promotes dual effects on bee behaviour and plant reproductive performance

Floral rewards do not only attract pollinators, but also herbivores and their predators. Ants are attracted by extrafloral nectaries (EFNs), situated near flowers, and may interfere with the efficiency and behaviour of pollinators. We tested the hypothesis that the impacts of ant–pollinator interactions in plant–pollinator systems are dependent on (1) the seasonal activity of EFNs, which increase ant abundance closer to flowers; (2) consequently, an ant effect, where ants decrease the temporal niche overlap of bees due to predator avoidance; and (3) ant density, where higher densities may negatively affect plant–pollinator interactions and plant performance. We studied two ant–plant–pollinator systems based on Banisteriopsis campestris and Banisteriopsis malifolia plant species. The periods of high ant abundance coincided with plant species blooming. The presence of ants around flowers reduced the visitation rates of the smaller bees and the temporal niche overlap between bee species was not higher than randomly expected when ants had free access. Additionally, we observed variable ant effects on fruit set and duration of bee visits to both Malpighiaceae species when ant density was experimentally kept constant on branches, especially on B. campestris. Our goal was to show the dual role of ant density effects, especially because the different outcomes are not commonly observed in the same plant species. We believe that reduced temporal niche overlap between floral visitors due to ant presence provides an opportunity for smaller bees to improve compatible pollination behaviour. Additionally, we concluded that ant density had variable effects on floral visitor behaviours and plant reproductive performance.     

Diurnal effectiveness of pollination by bees and flies in agricultural Brassica rapa: Implications for ecosystem resilience

Bees are known to provide pollination services to a wide range of crops, yet flies are rarely included in estimates of function. As bees and flies differ markedly in their life history characteristics and resource needs, they may be active and hence provide pollination services at different times of the day. Here, we explore the differences in bee and fly diurnal activity patterns and how this may impact upon pollination services provided to Brassica rapa, a mass-flowering crop. We observed pollinators at two-hourly intervals from 6:00 to 20:00 h in twelve fields in New Zealand in 2004–2005. Overall, bees were most active in the middle of the day and were more effective pollinators than flies, driven primarily by the high pollinator efficiency of Apis mellifera and Bombus terrestris. Some fly taxa however, visited flowers early and late in the day when there were few bees. The results of this study demonstrate that fine-scale temporal dynamics and the spatial distribution of crop pollinators may directly affect the quantity of pollination services. The maintenance of biodiversity in agro-ecosystems may therefore be critical to ensure pollinator taxa are available under a range of environmental conditions.     

Bee pollination of the endangered orchid Calanthe discolor through a generalized food-deceptive system

Calanthe discolor is a Japanese terrestrial orchid that is cultivated for its beautiful flowers arranged in racemose inflorescences. Although its propagation for horticultural purposes has been studied extensively resulting in the successful production of seedlings, little is known about the pollinators and breeding system of C. discolor in its natural habitat. The current study, which combined field observations and pollination experiments, was conducted to gain further insight into the reproduction of this important orchid species. Three bee species: Eucera nipponensis, Osmia cornifrons and Apis cerana japonica, were found to be effective pollinators, transferring the pollinaria on their heads. Pollination experiments also revealed that this species was self-compatible, although it was neither autogamous nor apogamous. The fruit set for the open-pollinated flowers was less than 10 %, suggesting a high degree of pollinator limitation, possibly as a result of the deceptive nature of this species. These results provide evidence that pollinator specificity is the primary mechanism of reproductive isolation between C. discolor and its close relative Calanthe striata, because the latter species is known to be exclusively pollinated by carpenter bee.     

Colour evolution within orchids depends on whether the pollinator is a bee or a fly

• Orchids are a classic angiosperm model for understanding biotic pollination. We studied orchid species within two species‐rich herbaceous communities that are known to have either hymenopteran or dipteran insects as the dominant pollinators, in order to understand how flower colour relates to pollinator visual systems.
• We analysed features of the floral reflectance spectra that are significant to pollinator visual systems and used models of dipteran and hymenopteran colour vision to characterise the chromatic signals used by fly‐pollinated and bee‐pollinated orchid species.
• In contrast to bee‐pollinated flowers, fly‐pollinated flowers had distinctive points of rapid reflectance change at long wavelengths and a complete absence of such spectral features at short wavelengths. Fly‐pollinated flowers also had significantly more restricted loci than bee‐pollinated flowers in colour space models of fly and bee vision alike.
• Globally, bee‐pollinated flowers are known to have distinctive, consistent colour signals. Our findings of different signals for fly pollination is consistent with pollinator‐mediated selection on orchid species that results from the distinctive features of fly visual systems.

     

The timing of food-deceptive flowers: a commentary on Internicola et al. (2008)

A recent article presents a study of pollinator visitation behaviour that is used to evaluate the selective pressure that pollinator visitation rate might have on the timing of the production of nonrewarding flowers. Here we take issue with the conclusions of the paper that there should be selection pressure for nonrewarding flowers to be available earlier in the season in order to avoid dissimilar sympatric rewarding species. Consideration of selection pressure must take into account temporal variation in total pollinator availability, pollinator longevity and unlearned response, and the stability of plant communities over time, as well as the learned responses of individual pollinators that the original study focused on. Learning alone would not necessarily select for early flowering by nonrewarders if temporal variation in pollinator numbers is strong or naïve pollinators consistently appear throughout the flowering season. Further, we argue that early flowering could simply be a natural corollary of longevity of flowers needed to combat negative frequency‐dependent selection and low overall visitation rates by pollinators, rather than a trait that has been specifically selected to reduce temporal overlap with competing rewarding species.     

Spatio‐temporal patterns in pollination of deceptive Aristolochia rotunda L. (Aristolochiaceae)

• Pollination success of highly specialised flowers is susceptible to fluctuations of the pollinator fauna. Mediterranean Aristolochia rotunda has deceptive trap flowers exhibiting a highly specialised pollination system. The sole pollinators are kleptoparasitic flies in search of food. This study investigates these pollinators on a spatio‐temporal scale and the impact of weather conditions on their availability. Two potential strategies of the plants to cope with pollinator limitation, i.e. autonomous selfing and an increased floral life span, were tested.
• A total of 6156 flowers were investigated for entrapped pollinators in 10 Croatian populations. Availability of the main pollinator was correlated to meteorological data. Artificial pollination experiments were conducted and the floral life span was recorded in two populations according to pollinator availability.
• Trachysiphonella ruficeps (Chloropidae) was identified as dominant pollinator, along with less abundant species of Chloropidae, Ceratopogonidae and Milichiidae. Pollinator compositions varied among populations. Weather conditions 15–30 days before pollination had a significant effect on availability of the main pollinator. Flowers were not autonomously selfing, and the floral life span exhibited considerable plasticity depending on pollinator availability.
• A. rotunda flowers rely on insect pollen vectors. Plants are specialised on a guild of kleptoparasitic flies, rather than on a single species. Pollinator variability may result in differing selection pressures among populations. The availability/abundance of pollinators depends on weather conditions during their larval development. Flowers show a prolonged trapping flower stage that likely increases outcrossing success during periods of pollinator limitation.

     

An exotic magnet plant alters pollinator abundance and behavior: a field test with a native mistletoe

Exotic species can threaten biodiversity by disrupting ecological interactions among native species. Highly-attractive exotic species can exert a ‘magnet effect’ by attracting native pollinators, which may have either competitive or facilitative effects on co-flowering native plants. However, those effects may be context-dependent. We used a mistletoe-hummingbird pollination system in the Valdivian rainforest (southern Chile) to test whether the exotic tree Eucalyptus globulus (a highly attractive species to pollinators) acts as a magnet species, affecting the co-flowering native mistletoe. We compared hummingbird abundance, visitation rates, and activity patterns between native forest and abandoned E. globulus plantations. We found that hummingbirds were more abundant and visited more flowers at the plantation irrespective of E. globulus flowering. We observed a significant change of pollinator activity at the native habitat during E. globulus flowering, as hummingbirds visited mistletoe flowers more frequently early in the morning at the plantations and in the afternoon at the native forests. Our results showed that E. globulus acts as an exotic magnet species and can alter pollinator abundance and behavior. Our findings demonstrate the importance of considering local- and landscape-scale processes to understand the effects of magnet species on native plants and suggest that magnet species may influence even highly-attractive plants.

     

The Potential Influence of Bumble Bee Visitation on Foraging Behaviors and Assemblages of Honey Bees on Squash Flowers in Highland Agricultural Ecosystems

Bee species interactions can benefit plant pollination through synergistic effects and complementary effects, or can be of detriment to plant pollination through competition effects by reducing visitation by effective pollinators. Since specific bee interactions influence the foraging performance of bees on flowers, they also act as drivers to regulate the assemblage of flower visitors. We selected squash (Cucurbita pepo L.) and its pollinators as a model system to study the foraging response of honey bees to the occurrence of bumble bees at two types of sites surrounded by a high amount of natural habitats (≥ 58% of land cover) and a low amount of natural habitats (≤ 12% of land cover) in a highland agricultural ecosystem in China. At the individual level, we measured the elapsed time from the departure of prior pollinator(s) to the arrival of another pollinator, the selection of honey bees for flowers occupied by bumble bees, and the length of time used by honey bees to explore floral resources at the two types of sites. At the community level, we explored the effect of bumble bee visitation on the distribution patterns of honey bees on squash flowers. Conclusively, bumble bee visitation caused an increase in elapsed time before flowers were visited again by a honey bee, a behavioral avoidance by a newly-arriving honey bee to select flowers occupied by bumble bees, and a shortened length of time the honey bee takes to examine and collect floral resources. The number of overall bumble bees on squash flowers was the most important factor explaining the difference in the distribution patterns of honey bees at the community level. Furthermore, decline in the number of overall bumble bees on the squash flowers resulted in an increase in the number of overall honey bees. Therefore, our study suggests that bee interactions provide an opportunity to enhance the resilience of ecosystem pollination services against the decline in pollinator diversity.