Managed bumble bees increase flower visitation but not fruit weight in polytunnel strawberry crops

Animal-mediated pollination is essential for the production and quality of fruits and seeds of many crops consumed by humans. However, crop pollination services might be compromised when wild pollinators are scarce. Managed pollinators are commonly used in crops to supplement such services with the assumption that they will enhance crop yield. However, information on the spatiotemporal pollinator-dependence of crops is still limited. We assessed the contribution of commercial bumble bee colonies compared to the available pollinator community on strawberry (‘Fortuna’ variety) flower visitation and strawberry quality across a landscape gradient of agricultural intensification (i.e. polytunnel berry crop cover). We used colonies of bumble bees in winter and in spring, i.e. when few and most wild pollinators are in their flight period, respectively. The placement of colonies increased visits of bumble bees to strawberry flowers, especially in winter. The use of bumble bee colonies did not affect flower visitation by other insects, mainly honey bees, hoverflies and other Diptera. Flower visitation by both honey bees and wild insects did not vary between seasons and was unrelated to the landscape gradient of berry crop cover. Strawberries were of the highest quality (i.e. weight) when insect-mediated pollination was allowed, and their quality was positively related to wild flower visitors in winter but not in spring. However, increased visits to strawberry flowers by managed bumble bees and honey bees had no effect on strawberry weight. Our results suggest that the pollination services producing high quality strawberry fruits are provided by the flower visitor community present in the study region without the need to use managed bumble bees.     

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.     

Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphanistrum

 We carried out two experiments to determine the effect of leaf damage on plant attractiveness to pollinators using wild radish, Raphanus raphanistrum (Brassicaceae), a self-incompatible annual herb. Pairs of plants from 36 full-sib families were grown in pots in the greenhouse. One member of each pair was damaged by Pieris rapae larvae that were allowed to remove half of the leaf area of each of the first four rosette leaves. The plants were subsequently taken out for pollinator observations once a week from the beginning of flowering in late June until the end of August. We conducted two experiments to examine how foliar damage affected visitation by pollinators. In the first experiment, numbers of pollinators visiting plants were compared between damaged and control sibling plants. In the second experiment, the number of open flowers during observations was controlled to be the same for both damaged and undamaged sibs. Damage significantly decreased the number and size of flowers during the first observations in late June. Damaged plants received fewer visits by native bees during the first week of observations. Since damage did not affect native bee visits when the number of open flowers was equalized between treatments, flower number was probably the main cue attracting native bees to plants. In the experiment without flower number control, syrphid flies, the other abundant pollinator taxon, spent more time per flower on the undamaged than on the damaged plants. When flower number was controlled, flies probed significantly more flowers during each visit on the undamaged than on the damaged plants and had higher visitation rates to undamaged plants early in the season. Since syrphid flies preferred undamaged plants both with and without flower number control, they apparently used cues apart from flower number for visitation. The difference between undamaged and damaged plants in floral characteristics and pollinator visitation vanished within a few weeks after the start of flowering. This result suggests that early damage may not have a strong fitness effect through reduction in mating success. However, poor weather conditions can cause early mortality of plants in the field, and nutrient depletion and competition decrease fruit set of later flowers. Therefore, conditions exist under which visitation to early flowers may affect plant fitness. Received: 30 July 1996 / Accepted: 10 February 1997     

REPRODUCTIVE BIOLOGY OF PETAL COLOR VARIANTS IN WILD POPULATIONS OF RAPHANUS SATIVUS: I. POLLINATOR RESPONSE TO COLOR MORPHS

Pollinator response to petal color polymorphism in wild radish (Raphanus sativus) was investigated. Behavior of insect visitors was observed within experimental flower arrays, each containing two of the petal color forms seen intermixed in California populations: white, yellow, pink, and bronze. Honeybees, which accounted for almost 90% of all visits, typically preferred yellow or white flowers and discriminated against bronze. Their preference for white increased significantly as the Raphanus flowering season progressed. Syrphid flies were also frequent visitors and increased in abundance near the end of the season. Syrphids typically preferred pink to other colors. Individual honeybees tended to specialize on either yellow or pink flowers on a short-term basis. This foraging pattern provides the potential for positive assortative mating among plants with yellow or pink flowers. Intraspecific pollinator discrimination may influence genotypic frequencies as well as the relative maternal and paternal reproductive success of color morphs.     

The effects of natural variation in pollinator visitation on rates of pollen removal in wild radish,Raphanus raphanistrum (Brassicaceae)

Pollen removal from flowers is an important component of male fitness, but the effects of natural variation in visitation rates on pollen removal are poorly understood. We measured pollen removal over 2 yr in experimental field populations of wild radish, Raphanus raphanistrum. Pollen removal and pollinator visitation over 1-hr periods were measured on previously unvisited flowers. The effects of pollen production and visitation by different insect taxa on pollen removal were determined using multiple regression. Pollen removal rates were extremely high; a median of 84% of pollen produced was removed in 1 hr. Pollen production was far more important than visitation in determining the number of pollen grains removed. Pollen removal increased with increasing numbers of visits by honey bees and small native bees, but increased numbers of syrphid fly visits had no effect. Average visit duration had no effect on pollen removal in 1991, and a marginally negative effect in 1992.     

Weed evolution after crop gene introgression: greater survival and fecundity of hybrids in a new environment

Crop-wild hybridization may produce offspring with lower fitness than their wild parents due to deleterious crop traits and outbreeding depression. Over time, however, selection for improved fitness could lead to greater invasiveness of hybrid taxa. To examine evolutionary change in crop-wild hybrids, we established four wild ( Raphanus raphanistrum ) and four hybrid radish populations ( R. raphanistrum  ×  Raphanus sativus ) in Michigan (MI), USA. Hybrid and wild populations had similar growth rates over four generations, and pollen fertility of hybrids improved. We then measured hybrid and wild fitness components in two common garden sites within the geographical range of wild radish [MI and California (CA)]. Advanced generation hybrids had slightly lower lifetime fecundity than wild plants in MI but exhibited c. 270% greater lifetime fecundity and c. 22% greater survival than wild plants in CA. Our results support the hypothesis that crop-wild hybridization may create genotypes with the potential to displace parental taxa in new environments.     

Bumble bee abundance and richness improves honey bee pollination behaviour in sweet cherry

Pollination service in agricultural crops increases significantly with pollinator diversity and wild pollinator abundance. Differences in the foraging behaviour of pollinating insects are one of the reasons why pollinator diversity and abundance enhances crop pollination. Here, we focused on the foraging behaviour of honey bees and bumble bees in sweet cherry orchards. In addition, we studied the influence of bee diversity and abundance on the foraging behaviour of honey bees and bumble bees. Honey bees were found to visit fewer flowers than bumble bees. Bumble bees also showed a higher probability of changing trees between rows than honey bees. Both visitation rate and probability of row changes of honey bees increased with bumble bee diversity and with bumble bee abundance. We also found that the probability of row changes of honey bees increased with increasing bumble bee abundance. These effects of bumble bee richness and abundance on the pollination behaviour of honey bees can improve the pollination performance of honey bees in crops that depend on cross pollination. Our results highlight the higher pollination performance of bumble bees and the facilitative effect of wild pollinators to crop pollination.     

Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brassicaceae)

Plant-pollinator interactions are one of the most important and variable mutualisms in nature. Multiple pollinators often visit plants and can vary in visitation rates, pollen removal and deposition, and spatial and temporal distribution, altering plant reproduction and patterns of pollinator-mediated selection. Although some visitors may not be effective pollinators, pollinator effectiveness is rarely estimated directly as seed set resulting from a single visit by each taxon visiting generalist plants. For two years, effectiveness of visitors to wild radish, Raphanus raphanistrum, was quantified by counting seeds set and pollen grains removed as a result of a single visit. We calculated a pollinator's importance to plant reproduction as the product of visitation rate and single-visit seed set, and regressed pollinator body size on pollen-removal and on seed set effectiveness. Although pollinators differed in effectiveness and visitation rates, pollinator importance was primarily determined by visitation rates. In contrast to similar 2-yr studies, pollinator assemblage composition varied little, suggesting pollinator-mediated selection can be consistent across years for this generalist. Larger pollinators were more effective than smaller at effecting seed set, but body size was a poor predictor of pollen removal ability. Instead, pollen-removal effectiveness may be more influenced by foraging behavior than size.     

Links between floral morphology and floral visitors along an elevational gradient in a Penstemon hybrid zone

Hybrid zones can form when two species of plants hybridize along an environmental gradient. Changes in floral morphology across such a gradient and the degree of reproductive isolation can be influenced by pollinator behavior, but little is known about pollinator visitation to hybridizing species that receive visits from a diverse array of animals. I studied floral morphology, nectar rewards and pollinator visitation for Penstemon newberryi , P. davidsonii and their hybrids along an elevational gradient in the Sierra Nevada of California. Sixty-two floral visitor species were observed visiting plants, making this system highly generalized compared to previous studies of visitation in hybrid zones. Morphological measurements were used to construct a plant hybrid index and examine the correlation with elevation and with floral visitors. Using observations of floral visitors along the gradient, I performed an ordination to determine whether the pollinator community changed along with plant morphology. Plants varied in a clinal pattern along the elevational gradient. The visitor community varied incrementally with altitude, although visitors to Penstemon davidsonii were separated from those to P. newberryi and hybrids along the main ordination axis. Hummingbirds were only found at low and middle elevations, and small halictid bees were relatively more abundant at high elevations. Although there is some potential for ecological isolation in the pollinator community, 11 common pollinator species visited both parent species and could be contributing to hybrid formation.     

Honey bees and wild pollinators differ in their preference for and use of introduced floral resources

Introduced plants may be important foraging resources for honey bees and wild pollinators, but how often and why pollinators visit introduced plants across an entire plant community is not well understood. Understanding the importance of introduced plants for pollinators could help guide management of these plants and conservation of pollinator habitat. We assessed how floral abundance and pollinator preference influence pollinator visitation rate and diversity on 30 introduced versus 24 native plants in central New York. Honey bees visited introduced and native plants at similar rates regardless of floral abundance. In contrast, as floral abundance increased, wild pollinator visitation rate decreased more strongly for introduced plants than native plants. Introduced plants as a group and native plants as a group did not differ in bee diversity or preference, but honey bees and wild pollinators preferred different plant species. As a case study, we then focused on knapweed (Centaurea spp.), an introduced plant that was the most preferred plant by honey bees, and that beekeepers value as a late‐summer foraging resource. We compared the extent to which honey bees versus wild pollinators visited knapweed relative to coflowering plants, and we quantified knapweed pollen and nectar collection by honey bees across 22 New York apiaries. Honey bees visited knapweed more frequently than coflowering plants and at a similar rate as all wild pollinators combined. All apiaries contained knapweed pollen in nectar, 86% of apiaries contained knapweed pollen in bee bread, and knapweed was sometimes a main pollen or nectar source for honey bees in late summer. Our results suggest that because of diverging responses to floral abundance and preferences for different plants, honey bees and wild pollinators differ in their use of introduced plants. Depending on the plant and its abundance, removing an introduced plant may impact honey bees more than wild pollinators.     

Different responses of pollinating bees to size variation and sexual phases in flowers ofCampanula

To examine the response of pollinating bees to size and sexual phases of flowers, we constructed an artificial population ofCampanula having large flower variation and presented it to potentially pollinating bees in nurseries. The pollinating bee groups (halictid, megachilid and bumble bees) responded differentially to both the flower size and to the sexual phases of the flowers. Whereas visitation rate of megachilid bees increased with the flower size, those of halictid bees and bumble bees did not show particular trends; for example, bumble bees visited almost all of the flowers consistently. Visitation frequencies to male-and female-phased flowers were significantly different between megachilids at Tokyo and halictids. This study indicates that pollinator attraction could not solely explain the evolution of the flower size inCampanula, and that other factors such as pollen transfer efficiency, should be considered.     

Bee- to bird-pollination shifts in <Emphasis Type="Italic">Penstemon</Emphasis>: effects of floral-lip removal and corolla constriction on the preferences of free-foraging bumble bees

Plants might be under selection for both attracting efficient pollinators and deterring wasteful visitors. Particular floral traits can act as exploitation barriers by discouraging the unwelcome visitors. In the genus Penstemon, evolutionary shifts from insect pollination to more efficient hummingbird pollination have occurred repeatedly, resulting in the convergent evolution of floral traits commonly present in hummingbird-pollinated flowers. Two of these traits, a reduced or reflexed lower petal lip and a narrow corolla, were found in a previous flight-cage study to affect floral handling time by bumble bees, therefore potentially acting as “anti-bee” traits affecting preference. To test whether these traits do reduce bumble bee visitation in natural populations, we manipulated these two traits in flowers of bee-pollinated Penstemon strictus to resemble hummingbird-adapted close relatives and measured the preferences of free-foraging bees. Constricted corollas strongly deterred bee visitation in general, and particularly reduced visits by small bumble bees, resulting in immediate specialization to larger, longer-tongued bumble bees. Bees were also deterred—albeit less strongly—by lipless flowers. However, we found no evidence that lip removal and corolla constriction interact to further affect bee preference. We conclude that narrow corolla tubes and reduced lips in hummingbird-pollinated penstemons function as exploitation barriers that reduce bee access to nectaries or increase handling time.     

Alien pollinator promotes invasive mutualism in an insular pollination system

The alien predatory lizard, Anolis carolinensis, has reduced the insect fauna on the two main islands of the Ogasawara archipelago in Japan. As a result of this disturbance, introduced honeybees are now the dominant visitors to flowers instead of endemic bees on these islands. On the other hand, satellite islands not invaded by alien anoles have retained the native flower visitors. The effects of pollinator change on plant reproduction were surveyed on these contrasting island groups. The total visitation rates and the number of interacting visitor groups on main islands were 63% and 30% lower than that on satellite islands, respectively. On the main islands, the honeybees preferred to visit alien flowers, whereas the dominant endemic bees on satellite islands tended to visit native flowers more frequently than alien flowers. These results suggest that alien anoles destroy the endemic pollination system and caused shift to alien mutualism. On the main islands, the natural fruit set of alien plants was significantly higher than that of native plants. In addition, the natural fruit set was positively correlated with the visitation rate of honeybees. Pollen limitation was observed in 53.3% of endemic species but only 16.7% of alien species. These data suggest that reproduction of alien plants was facilitated by the floral preference of introduced honeybees.     

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.     

Site-to-site differences in pollinator visitation patterns in a Louisiana iris hybrid zone

We studied pollinator visitation rates and movement patterns in experimental arrays of irises at two sites within a Louisiana iris hybrid zone. Arrays contained single-flowered stems of red-flowered I. fulva , blue-flowered I. hexagona , and purple-flowered F1 hybrids. At one site, where I. hexagona was the only wild-growing iris, queen bumble bees were the most common pollinator, and the rank order of pollinator visit rates was I. hexagona I. fulva . At a second site, where I. fulva predominated in the wild, hummingbirds were the most common pollinators, and this order was reversed: I. hexagona 相似文献   

Habitat structure and animal movement: the behaviour of bumble bees in uniform and random spatial resource distributions

Foraging organisms (like bumble bees) move between resource points (like flowers) whose natural distributions vary enormously: from hyperdispersed to random to clumped. These differences in habitat structure may significantly influence the fitness of both plant and pollinator. To examine the effect of habitat structure on pollinator movement and fitness, we observed captive worker bumble bees collecting nectar from artificial flowers containing equal volumes of reward and arranged in two spatial configurations: a hexagonal array with constant distances between flowers (“constant”), and an “exploded hexagonal” array, with variable distances between flowers (“variable”). The mean nearest-neighbour distance was the same in both arrays, as was the general hexagonal appearance. The experiment therefore compares how resource dispersion, independent of nearest-neighbour distance, influences bee behaviour. Bees in the variable array showed decreased directionality, higher revisitation frequencies, and greater inter-flower flight distances than shown in the constant array. As a consequence, bees in the variable array had a 19% lower gross rate of nectar collection. Our results suggest that wild-foraging bees should prefer regularly spaced flowers (when all else, including mean nearest-neighbour distance, is equal), and that plants can decrease self-pollination by regular spacing between flowers, inflorescences, or individuals. Received: 16 January 1996 / Accepted: 30 June 1997     

Pollination efficiency and foraging behaviour of honey bees and non‐Apis bees to sweet cherry

1. Crop pollination generally increases with pollinator diversity and wild pollinator visitation. To optimize crop pollination, it is necessary to investigate the pollination contribution of different pollinator species. In the present study, we examined this contribution of honey bees and non‐Apis bees (bumble bees, mason bees and other solitary bees) in sweet cherry.
2. We assessed the pollination efficiency (fruit set of flowers receiving only one visit) and foraging behaviour (flower visitation rate, probability of tree change, probability of row change and contact with the stigma) of honey bees and different types of non‐Apis bees.
3. Single visit pollination efficiency on sweet cherry was higher for both mason bees and solitary bees compared with bumble bees and honey bees. The different measures of foraging behaviour were variable among non‐Apis bees and honey bees. Adding to their high single visit efficiency, mason bees also visited significantly more flower per minute, and they had a high probability of tree change and a high probability to contact the stigma.
4. The results of the present study highlight the higher pollination performance of solitary bees and especially mason bees compared with bumble bees and honey bees. Management to support species with high pollination efficiency and effective foraging behaviour will promote crop pollination.

     

Limited phenological and pollinator-mediated isolation among selfing and outcrossing Arabidopsis lyrata populations

Transitions from outcrossing to selfing have been a frequent evolutionary shift in plants and clearly play a role in species divergence. However, many questions remain about the initial mechanistic basis of reproductive isolation during the evolution of selfing. For instance, how important are pre-zygotic pre-pollination mechanisms (e.g. changes in phenology and pollinator visitation) in maintaining reproductive isolation between newly arisen selfing populations and their outcrossing ancestors? To test whether changes in phenology and pollinator visitation isolate selfing populations of Arabidopsis lyrata from outcrossing populations, we conducted a common garden experiment with plants from selfing and outcrossing populations as well as their between-population hybrids. Specifically, we asked whether there was isolation between outcrossing and selfing plants and their between-population hybrids through differences in (1) the timing or intensity of flowering; and/or (2) pollinator visitation. We found that phenology largely overlapped between plants from outcrossing and selfing populations. There were also no differences in pollinator preference related to mating system. Additionally, pollinators preferred to visit flowers on the same plant rather than exploring nearby plants, creating a large opportunity for self-fertilization. Overall, this suggests that pre-zygotic pre-pollination mechanisms do not strongly reproductively isolate plants from selfing and outcrossing populations of Arabidopsis lyrata.     

Predicting patterns of mating and potential hybridization from pollinator behavior

Hybridization in flowering plants is determined in part by the rate at which animal pollinators move between species and by the effectiveness of such movements in transferring pollen. Pollinator behavior can also influence hybrid fitness by determining receipt and export of pollen. We incorporated information on pollinator effectiveness and visitation behavior into a simulation model that predicts pollen transfer between Ipomopsis aggregata, Ipomopsis tenuituba, and hybrids. These predictions were compared with estimates of pollen transfer derived from movement of fluorescent dyes in experimental plant arrays. Interspecific pollen transfer was relatively uncommon in these arrays, whereas transfer between hybrids and the parental species was at least as common as conspecific transfer. Backcrossing was asymmetrical; I. aggregata flowers frequently received mixed loads of hybrid and conspecific pollen. The simulation suggests that these patterns of pollen transfer are largely explained by the visitation sequences of hummingbird and insect pollinators, with little contribution from mechanical isolation. Pollen receipt by hybrids exceeded that of both parental species in a year when pollinators preferred to visit F(1) and F(2) hybrids and was intermediate in another year when they preferred to visit I. aggregata. This suggests that natural variation in pollination may produce spatiotemporal variation in hybridization and hybrid fitness.     

Competition alters life history and increases the relative fecundity of crop-wild radish hybrids (Raphanus spp.)

The evolutionary impact of crop-to-wild gene flow depends on the fitness of hybrids under natural, competitive conditions. Here, we measured the performance of third-generation (F3) radish hybrids (Raphanus raphanistrum x Raphanus sativus) and weedy R. raphanistrum to understand how competitive interactions affect life history and relative fecundity. Three wild and three F1 crop-wild hybrid radish populations were established in semi-natural, agricultural conditions in Michigan, USA. The effects of competition on life-history traits and fecundity of F3 progeny were measured 2 yr later in a common garden experiment. Third-generation hybrid plants generally produced fewer seeds per fruit and set fewer fruits per flower than wild plants, resulting in lower lifetime fecundity. With increasing competition, age at reproduction was delayed, the relative number of seeds per fruit was reduced in wild plants and differences between hybrid and wild fecundity diminished. Competition may enhance the fecundity of advanced-generation hybrids relative to wild plants by reducing differences in life history, potentially promoting the introgression of crop alleles into weed populations.