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.     

Honey bee (Hymenoptera: Apidae) distribution and potential for supplementary pollination in commercial tomato greenhouses during winter

This study examined the use of honey bees, Apis mellifera L., to supplement bumble bee, Bombus spp., pollination in commercial tomato, Lycopersicon esculentum Miller, greenhouses in Western Canada. Honey bee colonies were brought into greenhouses already containing bumble bees and left for 1 wk to acclimatize. The following week, counts of honey and bumble bees foraging and flying throughout the greenhouse were conducted three times per day, and tomato flowers open during honey bee pollination were marked for later fruit harvest. The same counts and flower-marking also were done before and after the presence of honey bees to determine the background level of bumble bee pollination. Overall, tomato size was not affected by the addition of honey bees, but in one greenhouse significantly larger tomatoes were produced with honey bees present compared with bumble bees alone. In that greenhouse, honey bee foraging was greater than in the other greenhouses. Honey bees generally foraged within 100 m of their colony in all greenhouses. Our study invites further research to examine the use of honey bees with reduced levels of bumble bees, or as sole pollinators of greenhouse tomatoes. We also make specific recommendations for how honey bees can best be managed in greenhouses.     

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.     

Effect of bumble bee (Hymenoptera: Apidae) pollination intensity on the quality of greenhouse tomatoes

Laboratory studies were conducted to assess tomato, Lycopersicon esculentum Mill. (Solanaceae), quality in relation to the level of buzz-pollination by bumble bees. Studies were conducted in commercial tomato greenhouses in the Leamington, Ontario, area to categorize bruising of tomato anther cones by bumble bees into five levels of bruising. The number of pollen grains per stigma was determined for each bruising level, and the bruising level was found to be a good predictor of stigmatic pollen load. Experimental flowers were pollinated by bumble bees and assigned to bruising levels based on the degree of anther cone discoloration. Fruit set, tomato weight, minimum diameter, the number of days until ripe, roundness, weight, percentage sugars, and number of seeds were assessed and compared among bruising level. Fruit set in flowers receiving no pollination visits was 30.2%, whereas, 83.3, 84.4, 81.2, and 100% of the flowers set fruit in bruising levels 1, 2, 3, and 4, respectively. Minimum diameter, number of seeds, and tomato weight all increased from no bruising to different levels of bruising. There was no increase in weight or diameter above a bruising level of 1, and no increase in the number of seeds per fruit after a bruising level of 2. We found that pollination of tomato flowers greater than a bruising level of 2 (corresponding to approximately one to two bee visits) did not result in a significant increase in quality.     

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.     

Evaluation of the neotropical stingless bee Melipona quadrifasciata (Hymenoptera: Apidae) as pollinator of greenhouse tomatoes

The Neotropical stingless bee Melipona quadrifasciata Lepeletier was evaluated for pollinating tomatoes (variety Rodas; long-life hybrid) in greenhouses under plastic and with a hydroponic system and "organic concepts" in Minas Gerais State, Brazil. Flowers not pollinated did not set any fruit. Pollination by bees plus manual pollination did not differ from either bee or manual pollination. Maximum fruit diameter, fruit height, and roundness (quotient between maximum fruit diameter and fruit height) were not significantly different between treatments, but fruit visited by M. quadrifasciata had 10.8% less seeds (dry mass) than manual pollination. This apparently low efficiency of M. quadrifasciata pollination was attributed to the overlap of only 30 min between highest bee foraging activity and highest flower stigma receptivity. Thus, it was concluded that M. quadrifasciata is a feasible pollinator of greenhouse tomatoes because of 1) the observed increase in fruit quality with lower mechanical injury than traditional manual pollination, 2) no significant decrease in fruit size, and 3) high price of such product in the market. Some considerations for sustainable use of M. quadrifasciata as greenhouse pollinator are presented. Although techniques for keeping captive colonies of M. quadrifasciata are currently available, the sole current method for acquiring new colonies is removing them from the forest, and if demand was created for large numbers of colonies for commercial use, techniques for captive rearing must be developed to prevent serious declines in wild populations.     

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.     

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.     

Pollinator genetics and pollination: do honey bee colonies selected for pollen‐hoarding field better pollinators of cranberry Vaccinium macrocarpon?

1. Genetic polymorphisms of flowering plants can influence pollinator foraging but it is not known whether heritable foraging polymorphisms of pollinators influence their pollination efficacies. Honey bees Apis mellifera L. visit cranberry flowers for nectar but rarely for pollen when alternative preferred flowers grow nearby. 2. Cranberry flowers visited once by pollen‐foraging honey bees received four‐fold more stigmatic pollen than flowers visited by mere nectar‐foragers (excluding nectar thieves). Manual greenhouse pollinations with fixed numbers of pollen tetrads (0, 2, 4, 8, 16, 32) achieved maximal fruit set with just eight pollen tetrads. Pollen‐foraging honey bees yielded a calculated 63% more berries than equal numbers of non‐thieving nectar‐foragers, even though both classes of forager made stigmatic contact. 3. Colonies headed by queens of a pollen‐hoarding genotype fielded significantly more pollen‐foraging trips than standard commercial genotypes, as did hives fitted with permanently engaged pollen traps or colonies containing more larvae. Pollen‐hoarding colonies together brought back twice as many cranberry pollen loads as control colonies, which was marginally significant despite marked daily variation in the proportion of collected pollen that was cranberry. 4. Caloric supplementation of matched, paired colonies failed to enhance pollen foraging despite the meagre nectar yields of individual cranberry flowers. 5. Heritable behavioural polymorphisms of the honey bee, such as pollen‐hoarding, can enhance fruit and seed set by a floral host (e.g. cranberry), but only if more preferred pollen hosts are absent or rare. Otherwise, honey bees' broad polylecty, flight range, and daily idiosyncrasies in floral fidelity will obscure specific pollen‐foraging differences at a given floral host, even among paired colonies in a seemingly uniform agricultural setting.     

Pollination of greenhouse tomatoes by the Australian bluebanded bee Amegilla (Zonamegilla) holmesi (Hymenoptera: Apidae)

The pollination effectiveness of bluebanded bees of the species Amegilla (Zonamegilla) holmesi Rayment (Hymenoptera: Apidae) was evaluated in tomato plants, Lycopersicon esculentum Miller (Solanaceae), cultivated in two greenhouse chambers. Bluebanded bee pollination was compared with mechanical pollination and no supplementary pollination. Pollination effectiveness was compared between treatments by using the percentage of fruit set, fruit weight, fruit diameter, fruit roundness, and the number of seeds per fruit. Both the bluebanded bee pollination and the mechanical pollination treatments significantly increased fruit set, individual fruit weight, and diameter compared with the control treatment. Fruit were also significantly rounder and contained significantly more seeds. Positive correlations were found for fruit weight versus seed number, maximum diameter versus seed number and minimum diameter versus seed number. We conclude that the use of A. holmesi for pollinating greenhouse tomatoes in Australia may be an effective alternative to the use of mechanical pollination.     

Key factors influencing forager distribution across macadamia orchards differ among species of managed bees

To achieve maximised and sustainable crop productivity, it is critical that we develop crop-specific strategies for managing pollination. Honey bees (Apis mellifera) and stingless bees (Tetragonula carbonaria) are considered effective pollinators of macadamia (Macadamia integrifolia). The introduction of managed honey bee or stingless bee hives into orchards is likely to boost the numbers of these insects visiting flowers; however, there is a lack of published information and consensus regarding their management for pollination. Here, we identify factors that affect the distribution of both honey bees and stingless bees across cultivated macadamia, and establish whether increased flower visitation leads to higher nut set. A gradient of bee visitation rates was created by placing colonies on the ends of a four-hectare block, and mixed-effect models were applied to assess forager abundance and nut set with respect to distance from hive, time of day, cultivar, and floral display size. Distance from colony had a strong effect on stingless bee numbers, with >96% of individuals recorded within 100 metres of colonies, whereas the distribution of honey bees was more closely related to daily floral display: trees with greater numbers of flowers attracted more honey bees. Simplified surveys conducted in a further 17 macadamia blocks confirm that these are broadly occurring distribution patterns. Bee abundance alone did not significantly predict nut production; however, an indirect effect of bee visits to flowers is inferred, as nut production increased with size of floral display. To encourage a more even distribution of bees and uniform pollination, we recommend placement of stingless bee hives to maximise their distribution through a block (e.g. at 100-m intervals) and management practices that promote even distributions of flowers across trees.     

Production of greenhouse tomatoes (Lycopersicon esculentum) using Nannotrigona perilampoides, Bombus impatiens and mechanical vibration (Hym.: Apoidea)

Importation of exotic bumblebees for greenhouse pollination may be restricted in México, thus making it necessary to evaluate the potential of native species as pollinators in enclosures. We studied the foraging activity and fruit production of tomato using one colony of Nannotrigona perilampoides (NP) and one colony of Bombus impatiens (BI) in greenhouses with ≈1000 plants. Mechanical vibration (MV) was included as a test treatment. The foraging activity was measured as the number of flowers visited within 5 min, the time spent on a flower collecting pollen, the number of visits that a flower received and the duration of a foraging trip. BI collected pollen more rapidly, visited more flowers within 5 min and did more visits per flower when compared with NP that also lasted longer in their trips. Significant correlations were found between environmental variables and the number of bees entering the hive and the number of bees on the flowers. For NP, the highest correlation was found for light intensity whilst in BI a negative effect of environmental temperature was detected. Regarding the quantity of fruit, BI resulted in higher fruit set when compared with NP, but the latter performed similarly to MV. However, the weight of the fruit and seed number was significantly higher for BI when compared with NP, and this was higher than for MV. Our results demonstrate that at the densities of tomato plants tested, one colony of BI was more efficient pollinator when compared with NP. We suggest that pollination efficiency of NP could have been limited by a reduced number of foragers on the plants at a given time and their limited flight range when compared with BI. Therefore, it will be necessary to evaluate if increasing densities of colonies of NP could improve tomato yield in tropical greenhouses.     

Comparative efficiency of Nannotrigona perilampoides, Bombus impatiens (Hymenoptera: Apoidea), and mechanical vibration on fruit production of enclosed habanero pepper

The native bee Nannotrigona perilampoides Cresson (Apidae: Meliponini) has been evaluated with promising results in greenhouse pollination of Solanaceae in Mexico. However, no comparison has been done with imported bumble bees (Apidae: Bombini), which are the most common bees used for greenhouse pollination. We compared the foraging activity and fruit production of habanero pepper. Capsicum chinense Jacquin, by using N. perilampoides and Bombus impatiens Cresson in pollination cages. Both bee species collected pollen on a similar number of flowers per unit time, but N. perilampoides visited significantly more flowers per trip, lasted longer on each flower, and spent more time per foraging trip. Ambient temperature and light intensity significantly affected the foraging activity of N. perilampoides. Light intensity was the only environmental variable that affected B. impatiens. Except for the fruit set, there were not significant differences in the quality of fruit produced by both bee species; however, N. perilampoides and B. impatiens performed better than mechanical vibration for all the variables measured. The abortion of fruit caused the low fruit set produced by B. impatiens, and we speculate it might be due to an excessive visitation rate. Pollination efficiency per visit (Spear's pollination efficiency index) was similar for both bee species in spite of the significantly lower amount of pollen removed by N. perilampoides. We suggested that the highest number of flowers visited per foraging trip coupled with adequate amounts of pollen transported, and transferred between flowers, could explain the performance of N. perilampoides as a good pollinator of habanero pepper. Our experiments confirm that N. perilampoides could be used as an alternative pollinator to Bombus in hot pepper under tropical climates.     

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.     

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.     

Pollination efficiencies of three bee (Hymenoptera: Apoidea) species visiting rabbiteye blueberry

Inadequate bee pollination limits rabbiteye blueberry, Vaccinium ashei Reade, production in the some areas of the southeastern United States. Honey bees, Apis mellifera L., are currently the only manageable pollinators available for pollinating V. ashei. However, a new adaptable pollinator for rabbiteye blueberry, Osmia ribifloris Cockerell, was successfully reared and flown in captivity. The bee nested successfully in wooden shelters and conferred superior fruit set to 2-yr-old potted, rabbiteye blueberry bushes. Pollination efficiency or the percentage of blueberry flowers to set fruit after being visited once by a female O. ribifloris was comparable to that of the female blueberry bee Habropoda laboriosa (F.) and worker honey bees. Interestingly, honey bees once thought to be inefficient pollinators of rabbiteye blueberry were found to be very efficient, especially for 'Climax' and 'Premier' flowers.     

Pollinating bees (Hymenoptera: Apiformes) of U.S. alfalfa compared for rates of pod and seed set

Alfalfa (=lucerne) flowers require visiting bees to trip the sexual column, thereby providing pollination and subsequent pod and seed set. Previous studies have compared the pollination values of different bee species solely by the speed with which they handle flowers and the proportion of visited flowers tripped. In this greenhouse study, five species of bees, including the three commercially managed U.S alfalfa pollinators, are likewise compared for their floral tripping frequencies. These bee species are also compared for the pod set and mature seed that results from their single visits to virgin flowers. Regardless of the identity of the pollinating bee, tripped flowers had the same probabilities of pod set and seed set. Thus, differences in the single-visit pollination efficiencies of the various bee species are entirely attributable to the proportion of visited flowers that they trip. Females of the alkali bee, Nomia melanderi Cockerell, and the alfalfa leafcutting bee, Megachile rotundata F, tripped 81 and 78% of visited flowers, respectively. Males of these species are significantly less effective (61 and 51%, respectively), but still significantly superior to the honey bee, Apis mellifera L. (22% of visited flowers tripped). These relationships are supported by field data for tripping frequencies. One candidate pollinator, Osmia sanrafaelae Parker, shows promise (44% tripped), but not the congeneric O. aglaia Sandhouse (13% tripped).     

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.     

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.     

Evaluation of an upper hive entrance for control of Aethina tumida (Coleoptera: Nitidulidae) in colonies of honey bees (Hymenoptera: Apidae)

This investigation was conducted to test whether an upper hive entrance may result in reduced Aethina tumida Murray (Coleoptera: Nitidulidae) population buildup in newly established honey bee, Apis mellifera L., colonies over an 8-mo period. The upper hive entrance consisted of a 3.5-cm-i.d. polyvinyl chloride pipe positioned 20 cm above the hive bottom. Sixteen bee colonies were established using five-frame nucleus hives with a 0.9-kg (2-1b) package of bees with queen. Eight colonies were placed in each apiary, and each colony received one of two treatments: 1) conventional hive lower entrance and 2) modified upper hive entrance. This investigation was conducted in two distant apiaries where A. tumida had been a major problem to local beekeepers for a minimum of 2 yr. Results showed no overall differences between treatment effects on A. tumida counts over the test period, but there was a reduction in bee brood measured in colonies having an upper hive entrance. We conclude that the upper pipe entrance is not recommended in areas where A. tumida are well established and have become problematic. The expected reduction of brood in colonies as a result of using an upper hive entrance will lead to less productive units for honey production and pollination activities. Other control measures will be necessary to maintain tolerable levels of A. tumida in honey bee colonies at high pest densities.