Managing honey bees (Hymenoptera: Apidae) for greenhouse tomato pollination

Although commercially reared colonies of bumble bees (Bombus sp.) are the primary pollinator world-wide for greenhouse tomatoes (Lycopersicon esculentum Mill.) previous research indicates that honey bees (Apis mellifera L.) might be a feasible alternative or supplement to bumble bee pollination. However, management methods for honey bee greenhouse tomato pollination scarcely have been explored. We 1) tested the effect of initial amounts of brood on colony population size and flight activity in screened greenhouses during the winter, and 2) compared foraging from colonies with brood used within screened and unscreened greenhouses during the summer. Brood rearing was maintained at low levels in both brood and no-brood colonies after 21 d during the winter, and emerging honey bees from both treatments had significantly lower weights than bees from outdoor colonies. Honey bee flight activity throughout the day and over the 21 d in the greenhouse was not influenced by initial brood level. In our summer experiment, brood production in screened greenhouses neared zero after 21 d but higher levels of brood were reared in unscreened greenhouses with access to outside forage. Flower visitation measured throughout the day and over the 21 d the colonies were in the greenhouse was not influenced by screening treatment. An economic analysis indicated that managing honey bees for greenhouse tomato pollination would be financially viable for both beekeepers and growers. We conclude that honey bees can be successfully managed for greenhouse tomato pollination in both screened and unscreened greenhouses if the foraging force is maintained by replacing colonies every 3 wk.     

Influence of brood, vent screening, and time of year on honey bee (Hymenoptera: Apidae) pollination and fruit quality of greenhouse tomatoes

Greenhouse tomatoes, Lycopersicon esculentum Miller (Solanaceae), are autogamous, but facilitated pollination results in increased fruit size and set. Previous research examining honey bee pollination in greenhouse tomato crops established that fruit quality resulting from honey bee visitation is often comparable to bumble bees (Bombus spp.) and significantly better than in flowers that receive no facilitated pollination. However, management alternatives have not been studied to improve tomato fruit quality when honey bees are the only pollination option available for the high-value greenhouse industry. We investigated whether the quantity of brood (eggs, larvae, and pupae) in a honey bee colony in the winter and screening on greenhouse vents in the summer would encourage honey bee foraging on tomato flowers. We also established the influence of time of year on the potential for honey bees to be effective pollinating agents. We constructed small honey bee colonies full of naive forager bees with either two frames of brood ("brood colonies") or two empty frames ("no-brood") and compared total fruit set and the number of tomato seeds resulting from fruit potentially visited by honey bees in each of these treatments to bagged flowers that received no facilitated pollination. There was no significant difference in the quality of fruit resulting from honey bees from "brood" and "no-brood" colonies. However, these fruits produced significantly more seeds than bagged flowers restricted from facilitated pollination. Honey bees from brood and no-brood colonies also resulted in 98% fruit set compared with 80% fruit set in bagged flowers that received no facilitated pollination. During the summer, the number of seeds per fruit did not differ significantly between unbagged flowers potentially visited by honey bees in screened greenhouses and unscreened greenhouses and bagged flowers that received no facilitated pollination. However, time of year did have a significant influence on the quality of fruit produced by honey bees compared with flowers that received no facilitated pollination, because no difference in seed number was observed between the treatments after mid-April. The results from this study demonstrate that the management of brood levels and vent screening cannot be used to improve the quality of fruit resulting from honey bee pollination and that honey bees can be a feasible greenhouse pollination alternative only during the winter.     

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.     

The habitat disruption induces immune-suppression and oxidative stress in honey bees

The honey bee is a major insect used for pollination of many commercial crops worldwide. Although the use of honey bees for pollination can disrupt the habitat, the effects on their physiology have never been determined. Recently, honey bee colonies have often collapsed when introduced in greenhouses for pollination in Japan. Thus, suppressing colony collapses and maintaining the number of worker bees in the colonies is essential for successful long-term pollination in greenhouses and recycling of honey bee colonies. To understand the physiological states of honey bees used for long-term pollination in greenhouses, we characterized their gene expression profiles by microarray. We found that the greenhouse environment changes the gene expression profiles and induces immune-suppression and oxidative stress in honey bees. In fact, the increase of the number of Nosema microsporidia and protein carbonyl content was observed in honey bees during pollination in greenhouses. Thus, honey bee colonies are likely to collapse during pollination in greenhouses when heavily infested with pathogens. Degradation of honey bee habitat by changing the outside environment of the colony, during pollination services for example, imposes negative impacts on honey bees. Thus, worldwide use of honey bees for crop pollination in general could be one of reasons for the decline of managed honey bee colonies.     

Behavior and pollination efficiency of Nannotrigona perilampoides (Hymenoptera: Meliponini) on greenhouse tomatoes (Lycopersicon esculentum) in subtropical México

The acclimation, foraging behavior, and pollination efficiency of stingless bees of the species Nannotrigona perilampoides Cresson were evaluated in tomato (Lycopersicon esculentum Mill.) plants cultivated in two greenhouses. The greenhouses were divided into three areas of 16 m2, and one of the following treatments was used for pollination: stingless bees (SB), mechanical vibration (MV), and no pollination (NP). Observations were conducted once a week from 0800 to 1600 hours during 2 mo. The acclimation of the bees to the greenhouses was estimated by the number of bees that did not return to the hive (lost bees) and by comparing the population of the colonies (brood and adults). The foraging activity of the bees across the day was evaluated by comparing the number of foragers per hour. The influence of environmental variables on the foraging activity was also analyzed. The pollination efficiency was compared among treatments through the percentage of fruit set, weight of individual fruit, kilograms of fruit produced per square meter, and the number of seed per fruit. The bees started foraging on the flowers approximately 7 d after the colonies were introduced to the greenhouse. There was a decline in the population of the colonies across the experiment, but colonies did not die out. Correlations of environmental variables with the foraging activity of the bees showed that none of them had a significant influence on pollen foraging. However, water collection was positively correlated with the temperature and negatively correlated with the humidity inside the greenhouse. The estimation of the pollination efficiency per treatment showed that there were significant differences in fruit set in SB (83 +/- 4.2) and MV (78.5 +/- 6.4) compared with NP (52.6 +/- 7.6). However, the average weight of the fruit was similar for the three treatments (65 g). There were significant differences for seed number in SB (200 +/- 15.3) and MV (232 +/- 21.4) compared with NP (120 +/- 16.6). The productivity in kilograms of fruit per square meter was higher in SB (5.72 +/- 0.61) and MV (5.66 +/- 0.58 kg) compared with NP (3.34 +/- 0.72). The number of seed was positively correlated with the weight of the fruit. We conclude that the use of Nannotrigona testaceicornis Rondani, for pollinating greenhouse tomatoes in tropical climates, could be an alternative to the use of highly defensive African-derived Apis mellifera or non-native bumble bees (Bombus spp.). However, more research is needed to evaluate the cost/benefit on large-scale greenhouse pollination using N. perilampoides Cresson against other bee species and pollination methods.     

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.     

Vectoring of Pepino mosaic virus by bumble‐bees in tomato greenhouses

Pepino mosaic virus (PepMV) has become an important viral disease of greenhouse tomatoes worldwide. The ability of bumble‐bees (Bombus impatiens), used for pollination, to acquire and transmit PepMV was investigated, and the prevalence of PepMV in plants and bumble‐bees in commercial tomato greenhouses was determined. PepMV infection in plants was determined using enzyme‐linked immunosorbent assay, while in bumble‐bees direct real‐time PCR was used. In the first experiment, the bumble‐bees were exposed for 14 days to PepMV‐infected plants. After 14 days, almost all bumble‐bees were PepMV positive both in the hive (78.5 ± 17.5%) and in the flowers (96.3 ± 3.6%). In the second experiment, bumble‐bees were released into a greenhouse with both PepMV‐infected source plants and healthy non‐infected target plants for 14 days. At the end of the experiment, 61.0 ± 19.5% of the bees collected from the hive and 83.3 ± 16.7% of the bees sampled from the flowers were PepMV positive. Bumble‐bees transmitted PepMV from the infected to the healthy non‐infected tomato plants. Two weeks after bumble‐bee release, the virus was detected in leaf, fruit and flower samples of formerly healthy plants. After 6 weeks, the percentage of PepMV positive samples from the target plants increased to 52.8 ± 2.8% of the leaves and 80.6 ± 8.4% of the fruits. In the control greenhouse without bumble‐bees, the target plants did not become infected. Based on the infection levels in flowers, fruits and leaves, the PepMV infection occurred possibly first in the pollinated flowers, and then spread from the fruit that developed from the flowers to other parts of the plant. In commercial greenhouses where PepMV was present, 92–100% of the plants and 88–100% of the bumble‐bees were PepMV positive. No infected plant samples were found in the control commercial greenhouse, but a small number of bumble‐bees (10%) tested PepMV positive.     

Farming practices influence wild pollinator populations on squash and pumpkin

Recent declines in managed honey bee, Apis mellifera L., colonies have increased interest in the current and potential contribution of wild bee populations to the pollination of agricultural crops. Because wild bees often live in agricultural fields, their population density and contribution to crop pollination may be influenced by farming practices, especially those used to reduce the populations of other insects. We took a census of pollinators of squash and pumpkin at 25 farms in Virginia, West Virginia, and Maryland to see whether pollinator abundance was related to farming practices. The main pollinators were Peponapis pruinosa Say; honey bees, and bumble bees (Bombus spp.). The squash bee was the most abundant pollinator on squash and pumpkin, occurring at 23 of 25 farms in population densities that were commonly several times higher than that of other pollinators. Squash bee density was related to tillage practices: no-tillage farms hosted three times as great a density of squash bees as tilled farms. Pollinator density was not related to pesticide use. Honey bee density on squash and pumpkin was not related to the presence of managed honey bee colonies on farms. Farms with colonies did not have more honey bees per flower than farms that did not keep honey bees, probably reflecting the lack of affinity of honey bees for these crops. Future research should examine the economic impacts of managing farms in ways that promote pollinators, particularly pollinators of crops that are not well served by managed honey bee colonies.     

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.

     

Bumble bee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato greenhouses

Commercial greenhouse studies were conducted to assess levels of pollination of tomato (Lycopersicon esculentum Mill.) flowers in relation to bumble bee (Bombus impatiens Cresson) colony activity and colony densities. For the assessment of pollination levels of tomato flowers, five categories were defined based on bruising levels caused by bumble bee pollination. Colony activity was measured as bee trips per ha/d using electric powered photodiode monitors inserted into the hive entrance. Levels of pollination were positively correlated with bee activity levels, up to a mean of approximately 400 pollen grains per stigma per day, after which greater activity did not result in further increases in daily pollination levels. Densities of colonies in the commercial greenhouses studied ranged from 7.6 to 19.8 colonies per hectare with a mean of 11.6 +/- 0.9. We found that an average activity of 2,000 bee trips per hectare per day was more than adequate to ensure sufficient pollination, and that this level of activity could be achieved with 7-15 colonies per hectare, depending on greenhouse conditions. Greenhouses requiring >15 colonies per hectare to achieve this level of pollination may be able to increase bee activity through alteration of greenhouse conditions. Across 50-m rows of tomato plants, levels of pollination decreased with increasing distance from bee colonies, suggesting that colonies should be evenly distributed throughout the greenhouses.     

Comparison and examination of Bombus occidentalis and Bombus impatiens (Hymenoptera: Apidae) in tomato greenhouses

Experiments were conducted in commercial tomato, Lycopersicon esculentum Miller (Solanaceae), greenhouses to compare the relative foraging effort of two bumble bee species, Bombus occidentalis Greene and Bombus impatiens Cresson, to examine interspecific competition between B. occidentalis and B. impatiens, and to determine whether bumble bee colonies grew to their full population potential in commercial tomato greenhouses. B. impatiens colonies had more brood and workers and made more foraging trips per hour than B. occidentalis colonies. However, B. impatiens returned to the colony without pollen loads and left their colonies without dropping off their pollen loads more frequently than B. occidentalis greenhouse colonies. Our data also suggest that the presence of B. impatiens had a detrimental effect on B. occidentalis populations. Furthermore, B. occidentalis colonies did not grow to their full population potential in tomato greenhouses, with fewer workers in greenhouse colonies than in colonies placed outside in a natural environment, or in colonies that were physically enclosed and protected from external mortality. Together, this study suggests that B. impatiens is a better pollinator than B. occidentalis. It also shows that unknown factors are limiting the size of B. occidentalis colonies in tomato greenhouses.     

Does Pathogen Spillover from Commercially Reared Bumble Bees Threaten Wild Pollinators?

The conservation of insect pollinators is drawing attention because of reported declines in bee species and the 'ecosystem services' they provide. This issue has been brought to a head by recent devastating losses of honey bees throughout North America (so called, 'Colony Collapse Disorder'); yet, we still have little understanding of the cause(s) of bee declines. Wild bumble bees (Bombus spp.) have also suffered serious declines and circumstantial evidence suggests that pathogen 'spillover' from commercially reared bumble bees, which are used extensively to pollinate greenhouse crops, is a possible cause. We constructed a spatially explicit model of pathogen spillover in bumble bees and, using laboratory experiments and the literature, estimated parameter values for the spillover of Crithidia bombi, a destructive pathogen commonly found in commercial Bombus. We also monitored wild bumble bee populations near greenhouses for evidence of pathogen spillover, and compared the fit of our model to patterns of C. bombi infection observed in the field. Our model predicts that, during the first three months of spillover, transmission from commercial hives would infect up to 20% of wild bumble bees within 2 km of the greenhouse. However, a travelling wave of disease is predicted to form suddenly, infecting up to 35-100% of wild Bombus, and spread away from the greenhouse at a rate of 2 km/wk. In the field, although we did not observe a large epizootic wave of infection, the prevalences of C. bombi near greenhouses were consistent with our model. Indeed, we found that spillover has allowed C. bombi to invade several wild bumble bee species near greenhouses. Given the available evidence, it is likely that pathogen spillover from commercial bees is contributing to the ongoing decline of wild Bombus in North America. Improved management of domestic bees, for example by reducing their parasite loads and their overlap with wild congeners, could diminish or even eliminate pathogen spillover.     

Bee visitation rates to cultivated sunflowers increase with the amount and accessibility of nectar sugars

Pollinators make foraging decisions based on numerous floral traits, including nectar and pollen rewards, and associated visual and olfactory cues. For insect‐pollinated crops, identifying and breeding for attractive floral traits may increase yields. In this study, we examined floral trait variation within cultivated sunflowers and its effects on bee foraging behaviours. Over 2 years, we planted different sunflower inbred lines, including male‐fertile and male‐sterile lines, and measured nectar volume, nectar sugar concentration and composition, and corolla length. During bloom, we recorded visits by both managed honey bees and wild bees. We then examined consistency in relative nectar production by comparing field results to those from a greenhouse experiment. Sunflower inbred lines varied significantly in all floral traits, including the amount and composition of nectar sugars, and in corolla length. Both wild bee and honey bee visits significantly increased with nectar sugar amount and decreased with corolla length, but appeared unaffected by nectar sugar composition. While wild bees made more visits to sunflowers providing pollen (male‐fertile), honey bees preferred plants without pollen (male‐sterile). Differences in nectar quantity among greenhouse‐grown sunflower lines were similar to those measured in the field, and bumble bees preferentially visited lines with more nectar in greenhouse observations. Our results show that sunflowers with greater quantities of nectar sugar and shorter corollas receive greater pollination services from both managed and wild bees. Selecting for these traits could thus increase sunflower crop yields and provide greater floral resources for bees.     

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.     

生态条件的多样性变化对蜜蜂生存的影响

蜜蜂在整个生态系统中起着重要的传花授粉作用,是生态链中不可或缺的物种。随着现代农业的发展,蜜蜂赖以生存的环境遭到破坏,继而引发蜜蜂数量大幅减少,影响了蜂种的生存与可持续发展。总结了近年来生态条件的变化,归纳了影响蜜蜂生存的主要因素,分析了蜜蜂生存艰难的原因,提出了蜜蜂生存的关键问题,并展望了未来维持蜜蜂强群的主要研究方向。     

Longer tongues and swifter handling: why do more bumble bees (Bombus spp.) than honey bees (Apis mellifera) forage on lavender (Lavandula spp.)?

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意大利蜜蜂和小峰熊蜂在温室桃园的传粉行为及其影响因素

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Population genetics of wild and managed pollinators: implications for crop pollination and the genetic integrity of wild bees

Loss of habitat and chemical use associated with agriculture can cause population declines of wild pollinators. Less is known about the evolutionary consequences of interactions between species used in commercial agriculture and wild pollinators. Given population declines of many wild bee species, it is crucial to understand if commercial queens become established in natural areas, if wild bees visit agricultural fields and have the potential to interact with commercial bees, and if gene flow occurs between commercial and wild bees. We drew on a long-term data set that documents commercial bumble bee (Bombus impatiens) use in New England, and we conducted genetic analyses of foraging B. impatiens from areas with varying intensities of commercial bee use. In agricultural areas with a history of commercial bee use we also sampled bees directly from commercial hives. We found significant genetic differences among foraging B. impatiens and B. impatiens sampled directly from hives (average pairwise F′_ST = 0.14), but not among samples of foraging bees from natural areas (average F′_ST among foraging bees?=?0.002). Furthermore, Bayesian analysis of population structure revealed that foraging bees caught in areas with a history of commercial bee use grouped with samples from natural areas. These results document an agricultural setting where there was no widespread introgression of alleles from commercial bumble bees to wild bumble bees, commercial bumble bees did not become established in natural areas, and wild bees were providing pollination services to crops.     

Orchard pollination in Capitol Reef National Park,Utah, USA. Honey bees or native bees?

Capitol Reef National Park in central Utah, USA surrounds 22 managed fruit orchards started over a century ago by Mormon pioneers. Honey bees are imported for pollination, although the area in which the Park is embedded has over 700 species of native bees, many of which are potential orchard pollinators. We studied the visitation of native bees to apple, pear, apricot, and sweet cherry over 2 years. Thirty species of bees visited the flowers but, except for pear flowers, most were uncommon compared to honey bees. Evidence that honey bees prevented native bees from foraging on orchard crop flowers was equivocal: generally, honey bee and native bee visitation rates to the flowers were not negatively correlated, nor were native bee visitation rates positively correlated with distance of orchards from honey bee hives. Conversely, competition was tentatively suggested by much larger numbers of honey bees than natives on the flowers of apples, apricots and cherry; and by the large increase of native bees on pears, where honey bee numbers were low. At least one-third of the native bee species visiting the flowers are potential pollinators, including cavity-nesting species such as Osmia lignaria propinqua, currently managed for small orchard pollination in the US, plus several fossorial species, including one rosaceous flower specialist (Andrena milwaukiensis). We suggest that gradual withdrawal of honey bees from the Park would help conserve native bee populations without decreasing orchard crop productivity, and would serve as a demonstration of the commercial value of native pollinators.