Bumblebee Workers Research Articles

Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees

AbstractPollination success of plants is highly susceptible to the frequency of visits and foraging behavior of pollinators. Pollination of the nectarless flowers of Pedicularis species depends on bumblebee workers collecting pollen by vibrating the anthers (buzz pollination). However, little is known about the efficiency of the pollination system. Foraging behavior, pollen removal from anthers and pollen deposition on stigmas of P. chamissonis were studied to assess the effectiveness of buzz pollination in an alpine snowbed population of northern Japan. Although bumblebees tended to visit most of the flowers open at a given time within inflorescences during a single visit, pollen removal rate at the first visit was about 20%, and buzzing period decreased with increasing number of previous visits, resulting in a decreasing proportion of pollen removed per visit as the number of visits increased. These trends enable plants to provide pollen for more pollinators. The number of pollen grains deposited on stigmas was not saturated during the first visit and increased with additional visits. Irrespective of weak self‐compatibility, evidence of interference between self and outcross pollen was lacking for seed production. Therefore, buzz pollination in P. chamissonis acts as a mechanism that improves the chance of cross‐pollination upon multiple visits if pollinator visitation is frequent.

Temporal variation in group aggressiveness of honeybee (Apis mellifera) guards

Little is known about the temporal organization of defensive behavior in honeybees. We studied “guards”, the best-characterized class of colony defenders. We synchronized small groups under a light-dark illumination regime (LD), and video recorded their aggression toward an intruder bumblebee worker. In 1 out of 3 trials (each trial with a different source colony), the latency before the first attack was longer during the night in LD, or subjective night in constant conditions (DD); a similar trend was observed in DD in the two other trials. In 2 out of 3 trials, the number of stinging attempts varied with highest levels during the day in DD, but not in LD. There was a similar trend for the number of biting events. These findings reveal temporal variation in aggression under constant conditions, consistent with the hypothesis that the circadian clock influences guard aggressiveness. Nevertheless, the variability between LD and DD and across colonies calls for additional studies before reaching a definitive conclusion.

Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size

Numerous studies suggest that honeybees may compete with native pollinators where introduced as non-native insects. Here we examine evidence for competition between honeybees and four bumblebee species in Scotland, a region that may be within the natural range of honeybees, but where domestication greatly increases the honeybee population. We examined mean thorax widths (a reliable measure of body size) of workers of Bombus pascuorum, B. lucorum, B. lapidarius and B. terrestris at sites with and without honeybees. Workers of all four species were significantly smaller in areas with honeybees. We suggest that reduced worker size is likely to have implications for bumblebee colony success. These results imply that, for conservation purposes, some restrictions should be considered with regard to placing honeybee hives in or near areas where populations of rare bumblebee species persist.

Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens)

Here we explored the potential for host shift from honeybee, Apis mellifera, colonies to bumblebee, Bombus impatiens, colonies by the small hive beetle, a nest parasite/scavenger native to sub-Saharan Africa. We investigated small hive beetle host choice, bumblebee colony defence as well as individual defensive behaviour of honeybee and bumblebee workers. Our findings show that in its new range in North America, bumblebees are potential alternate hosts for the small hive beetle. We found that small hive beetles do invade bumblebee colonies and readily oviposit there. Honeybee colonies are not preferred over bumblebee colonies. But even though bumblebees lack a co-evolutionary history with the small hive beetle, they are able to defend their colonies against this nest intruder by removal of beetle eggs and larvae and stinging of the latter. Hence, the observed behavioural mechanisms must be part of a generalistic defence system suitable for defence against multiple attackers. Nevertheless, there are quantitative (worker force) and qualitative differences (hygienic behaviour) between A. mellifera and B. impatiens.

Impact of insecticidal proteins expressed in transgenic plants on bumblebee microcolonies

AbstractIn order to assess the risk that insecticidal transgenic plants may pose for bumblebees, we tested whether Bombus terrestris (L.) (Hymenoptera: Apidae) workers are able to detect insecticidal proteins dissolved in sucrose solution and whether consumption of these proteins will affect survival and offspring production. Feeders containing either Bacillus thuringiensis toxin (Cry1Ab), Kunitz soybean trypsin inhibitor (SBTI), or Galanthus nivalis agglutinin (GNA) were offered to bumblebee colonies at low (0.01% wt/vol for SBTI and GNA, 0.001% for Cry1Ab) and high concentrations (0.1% for SBTI and GNA, 0.01% for Cry1Ab) together with a control (pure sucrose solution) in a glasshouse chamber. No difference was found in the number of visits and the duration of visits among the different concentrations for each of the insecticidal proteins, indicating that bumblebees do not discriminate the compounds. To investigate the impact of the different insecticidal proteins on B. terrestris, microcolonies were established by placing three newly emerged bumblebee workers in wooden boxes. Within a few days, a hierarchy in each microcolony was established and the dominant worker developed its ovaries and laid haploid eggs. Bumblebees were fed with Cry1Ab (0.01%), SBTI, or GNA (both at 0.01 and 0.1%) dissolved in sucrose solution and also fed mixed floral pollen for a maximum period of 80 days. Additionally, microcolonies with three drones each were established to measure individual bee longevity. While the Cry1Ab did not affect microcolony performance, the consumption of SBTI and especially GNA affected survival of B. terrestris workers and drones and caused a significant reduction in the number of offspring. The use of microcolonies appears to be well‐suited to measure lethal and sublethal effects of insecticidal proteins expressed in transgenic plants on bumblebees.

Commercial colonies of Bombus terrestris (Hymenoptera: Apidae) are reservoirs of the tracheal mite Locustacarus buchneri (Acari: Podapolipidae)

We investigated the prevalence of infestation by the bumblebee tracheal mite, Locustacarus buchneri (Acari: Podapolipidae), in four commercial colonies of Bombus terrestris (Hymenoptera: Apidae). All the foundresses, 91.8±5.67% (mean±SE) of worker bees, 73.9±6.85% of males, and 77.4±21.5% of new queens had the mite in their abdominal air sacs. The mean number of eggs, adult females, and mobile mites infesting a single bumblebee worker were 76.9±76.8 (range: 4–301, n=40), 3.78±3.45 (1–11, 40), and 3.45±2.98 (1–11, 20), respectively. From these values, we calculated the number of eggs per adult mite female to be 23.9±21.7 (range: 4–126, n=40). As a single worker bee had about 76 mites in her abdominal air sacs and approximately 90% of the bees in a colony of about 160 bees were infested by the mite, an infested B. terrestris colony has the potential to produce more than 10,000 L. buchneri individuals during colony development.

Foraging scent marks of bumblebees: footprint cues rather than pheromone signals

In their natural habitat foraging bumblebees refuse to land on and probe flowers that have been recently visited (and depleted) by themselves, conspecifics or other bees, which increases their overall rate of nectar intake. This avoidance is often based on recognition of scent marks deposited by previous visitors. While the term 'scent mark' implies active labelling, it is an open question whether the repellent chemicals are pheromones actively and specifically released during flower visits, or mere footprints deposited unspecifically wherever bees walk. To distinguish between the two possibilities, we presented worker bumblebees (Bombus terrestris) with three types of feeders in a laboratory experiment: unvisited control feeders, passive feeders with a corolla that the bee had walked over on its way from the nest (with unspecific footprints), and active feeders, which the bee had just visited and depleted, but which were immediately refilled with sugar-water (potentially with specific scent marks). Bumblebees rejected both active and passive feeders more frequently than unvisited controls. The rate of rejection of passive feeders was only slightly lower than that of active feeders, and this difference vanished completely when passive corollas were walked over repeatedly on the way from the nest. Thus, mere footprints were sufficient to emulate the repellent effect of an actual feeder visit. In confirmation, glass slides on which bumblebees had walked on near the nest entrance accumulated hydrocarbons (alkanes and alkenes, C23 to C31), which had previously been shown to elicit repellency in flower choice experiments. We conclude that repellent scent marks are mere footprints, which foraging bees avoid when they encounter them in a foraging context.

Reproductive plasticity in bumblebee workers (Bombus terrestris)—reversion from fertility to sterility under queen influence

Worker sterility in the bumblebee Bombus terrestris is conditional and is linked to the social development of the colony. Workers refrain from reproducing or overtly challenging the queen until gyne production has initiated, at the so-called competition point (CP). It is not known whether this behavior is hard-wired or workers show reproductive plasticity. It also remains unclear whether worker reproductive decision is under queen and/or worker control. In this study, we tested worker reproductive plasticity in an attempt to assess whether and under which conditions worker sterility/fertility are reversible. We introduced egg-laying workers into colonies with different social structures for 1 week then monitored their reproductive status. We revealed a remarkable reproductive plasticity in the introduced workers that was social-condition-dependent. In the presence of a pre-CP queen, the introduced workers reverted to sterility, whereas in the presence of a post-CP queen, such workers remained egg-layer. Reversion to sterility does not occur when direct contact with the queen is prevented, as the introduced workers remained egg-layer in the queenright colonies with a confined queen. Egg-laying workers that were introduced into queenless colonies mostly maintained their fertility regardless of colony social phase. This shows that worker transition from cooperative to selfish behavior is reversible depending on the social context.

Variability in Floral Scent in Rewarding and Deceptive Orchids: The Signature of Pollinator-imposed Selection?

A comparative investigation was made of floral scent variation in the closely related, food-rewarding Anacamptis coriophora and the food-deceptive Anacamptis morio in order to identify patterns of variability of odour compounds in the two species and their role in pollinator attraction/avoidance learning. Scent was collected from plants in natural populations and samples were analysed via quantitative gas chromatography and mass spectrometry. Combined gas chromatography and electroantennographic detection was used to identify compounds that are detected by the pollinators. Experimental reduction of scent variability was performed in the field with plots of A. morio plants supplemented with a uniform amount of anisaldehyde. Both orchid species emitted complex odour bouquets. In A. coriophora the two main benzenoid compounds, hydroquinone dimethyl ether (1,4-dimethoxybenzene) and anisaldehyde (methoxybenzaldehyde), triggered electrophysiological responses in olfactory neurons of honey-bee and bumble-bee workers. The scent of A. morio, however, was too weak to elicit any electrophysiological responses. The overall variation in scent was significantly lower in the rewarding A. coriophora than in the deceptive A. morio, suggesting pollinator avoidance-learning selecting for high variation in the deceptive species. A. morio flowers supplemented with non-variable scent in plot experiments, however, did not show significantly reduced pollination success. Whereas in the rewarding A. coriophora stabilizing selection imposed by floral constancy of the pollinators may reduce scent variability, in the deceptive A. morio the emitted scent seems to be too weak to be detected by pollinators and thus its high variability may result from relaxed selection on this floral trait.

Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers

The eusocial bumblebees exhibit pronounced size variation among workers of the same colony. Differently sized workers engage in different tasks (alloethism); large individuals are found to have a higher probability to leave the colony and search for food, whereas small workers tend to stay inside the nest and attend to nest duties. We investigated the effect of size variation on morphology and physiology of the peripheral olfactory system and the behavioral response thresholds to odors in workers of Bombus terrestris. Number and density of olfactory sensilla on the antennae correlate significantly with worker size. Consistent with these morphological changes, we found that antennal sensitivity to odors increases with body size. Antennae of large individuals show higher electroantennogram responses to a given odor concentration than those of smaller nestmates. This finding indicates that large antennae exhibit an increased capability to catch odor molecules and thus are more sensitive to odors than small antennae. We confirmed this prediction in a dual choice behavioral experiment showing that large workers indeed are able to respond correctly to much lower odor concentrations than small workers. Learning performance in these experiments did not differ between small and large bumblebees. Our results clearly show that, in the social bumblebees, variation in olfactory sensilla number due to size differences among workers strongly affects individual odor sensitivity. We speculate that superior odor sensitivity of large workers has favored size-related division of labor in bumblebee colonies.

The pollination ecology of Pedicularis rex subsp . lipkyana and P. rex subsp. rex (Orobanchaceae) from Sichuan, southwestern China

Pedicularis is one of few genera for which pollination ecology has been studied extensively. Although over half of the species of Pedicularis are found in the mountains of southwestern China, pollination ecology has been studied there on a few species only. The present paper reports pollination ecology of Pedicularis rex subsp. lipskyana and P. rex subsp. rex from Sichuan, southwestern China. The two subspecies are nectariferous, with sugar content 28% in P. rex lipskyana and 22% in P. rex, respectively. The flowers of the two subspecies are adapted to pollination by bumblebee workers. Bumblebees are the primary and effective pollinators although honeybees were also observed pollinating P. rex subsp. lipskyana at one studied population. Usually bumblebees entered the corolla tube from the right side in an upright or a nearly half-inverted position to imbibe nectar located at the base of the corolla tube. The stigma usually contacts the side region of the thorax and abdomen or occasionally directly contacted pollen loads, leading to pollination of flowers. Much less commonly, bumblebees foraged on flowers of P. rex subsp. rex in an inverted position for pollen, which pollinated flowers sternotribically. We suggest that pollination mechanism is closely associated with floral morphology. Some important differences were found from a previous study on P. rex in floral morphology and the primary pollination mechanism.

Effect of Group Size on Ovarian Development in Bumblebee Workers (Hymenoptera: Apidae: Bombus)

CNAANI J, WONG A & THOMSON J D [Dep Zool, Univ Toronto, Ont, Canada]: Effect of Group Size on Ovarian Development in Bumblebee Workers (Hymenoptera: Apidae: Bombus). - Entomol Gener 29(2/4): 305-314; Stuttgart 2007-01. --- [Note] Isolated bumblebee workers. Bombus impatiens Cresson 1863, developed their ovaries to produce laying-sized eggs in 11 days, but did so 5 days faster in queenless groups of 2-12 that they came to dominate. In groups larger than pairs, reproductive dominance (as measured by oocyte length) was distributed continuously in a graded hierarchy, rather than dichotomously. In groups, workers at a particular dominance rank position developed larger oocytes as group size increased, indicating that a focal bee's stimulus for reproductive development depends on the number of other bees that are subordinate to it. Attempts to relate ovarian development to visible behavioral manifestations of dominance were inconclusive because antagonistic interaction were infrequent.

Modification of the Innate Antennal Reaction at Floral Guides in Experienced Bumblebees, Bombus terrestris (Hymenoptera: Apidae)

The first physical contact with flowers by flower-naive bumblebees of the species Bombus terrestris (Linnaeus 1758) is a touch with the tips of their antennae prior to landing. Naive bumblebees perform this innate antennal reaction either at the margin of flowers or at small coloured floral guides. LUNAU [1992] hypothesised that the antennal reaction aims at the perception of substances on floral tissues through chemoreception. In order to test the effect of experience with distinct flower guides on the antennal reaction learning experiments were performed with worker bumblebees of the species Bombus terrestris. A choice of two types of artificial flowers was presented simultaneously: (1) Blue artificial flowers with a small central yellow colour mark, offering 7 μl of 50% sucrose solution, and (2) blue artificial flowers with a small central brown colour mark, offering 7 μl of 10% sucrose solution. The antennal reaction of individuals was monitored at two different phases in the experiment: (1) During the first 90 approaches, and (2) after 300 approaches to artificial flowers. Unexpectedly it was found that experienced bumblebees showed the antennal reaction significantly more often at the small central colour mark than less experienced ones. During flight, bumblebees retained the antennae in a position characterised by a distance between the antennal tips of more than 5 mm and by an angle between the antennal flagella of more than 90°. Prior to antennal contact with the artificial flower experienced bumblebees reduced the distance between the antennal tips to about 5 mm, which corresponds to the diameter of the central colour mark. This adjustment was not dependent on the presence of scent-marks. It is suggested that bumblebees benefit from their antennal reaction at flowers by remote sensing of pollen reward and consequential avoidance of waste of energy by landing and restarting from the flower.

Influence of scent deposits on flower choice: experiments in an artificial flower array with bumblebees

Foraging bumblebees leave chemical substances when visiting flowers and the detection of these “scent marks” improves their foraging efficiency. Whereas laboratory studies found that scent-marks convey attraction to food sources, all field studies found foragers to be repelled by recently visited flowers. In this study we aim to resolve this conflict by implementing near-natural reward dynamics in a laboratory feeder array. When feeders were filled with small, non-replenished amounts of reward, worker bumblebees (Bombus terrestris) avoided revisiting the depleted feeders. As evidenced by a “corolla” replacement experiment, feeder discrimination was based on the perception of chemical cues deposited during previous visits. Pentane extracts of bumblebee tarsi acted as a repellent when applied to glass corollas, whereas pure pentane did not. We suggest that scent-marks are simple cues inherent to footprints and emphasize the importance of context to how these cues are interpreted by foraging bees.

Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida)

Abstract 1. The small hive beetle, Aethina tumida, is a parasite of honeybee (Apis mellifera) colonies native to sub‐Saharan Africa and has become an invasive species. In North America the beetle is now sympatric with bumblebees, Bombus, not occurring in its native range. Laboratory studies have shown that small hive beetles can reproduce in bumblebee colonies but it was not known whether infestations occur in the field.2. For the first time, infestation of bumblebee colonies by small hive beetles was investigated in the field. Commercial Bombus impatiens colonies (n= 10) were installed in proximity to infested apiaries. Within 8 weeks, all colonies that were alive in the 5‐week observation period (n= 9) became naturally infested with adult small hive beetles and successful small hive beetle reproduction occurred in five colonies.3. In four‐square choice tests, the beetles were attracted to both adult bumblebee workers and pollen from bumblebee nests, suggesting that these odours may serve as cues for host finding.4. The data indicate that bumblebee colonies may serve as alternative hosts for small hive beetles in the field. To foster the conservation of these essential native pollinators, investigations on the actual impact of small hive beetles on wild bumblebee populations are suggested.

New method to stimulate the onset of Bombus terrestris (Hymenoptera: Apidae) rearing: Using worker helpers in the presence of frozen pupae

AbstractThe failure of bumblebee queens to enthusiastically start a colony under laboratory conditions may be due to lack of oviposition during an experiment, a long delay in oviposition from the termination of hibernation, and failure to rear a large first brood. In the present study, the use of frozen male pupae to start the colony with the assistance of bumblebee workers rather than fresh, young, male pupae was investigated under controlled room temperature and humidity conditions. The period of initiation of the colony decreased with an increase in the number of worker helpers from one to six. The period was as short as 3.9 days in the presence of six worker helpers. Second and third broods also started earlier with the help of workers. The rate of first worker production per egg cup was double that of the normal method (i.e. without worker helpers). Egg eating behavior of the queen was not found in the first brood if more than two workers helped the development of the larvae. Four worker helpers were found to be sufficient, as they could produce 100% colony foundation and 91.46% first worker production colonies. This study showed that using frozen old pupae is a good stimulator for colony foundation in the presence of four bumblebee worker helpers.

Bumblebees can be used in combination with juvenile hormone analogues and ecdysone agonists

This study examined the lethal and sublethal effects on the beneficial insect Bombus terrestris by two classes of insect growth regulators (IGRs) that are commercially used in agriculture to control pest insects. Three juvenile hormones analogues (JHAs) (pyriproxyfen, fenoxycarb and kinoprene) and two ecdysone agonists or moulting accelerating compounds (MACs) (tebufenozide and methoxyfenozide) were tested. The bumblebee workers were exposed to the insecticides via three different routes of exposure: dermally by topical contact, and orally via the drinking sugar water or the pollen. In the first series of experiments the IGRs were applied at their respective maximum field recommended concentration (MFRC). These risk hazard tests showed that the tested IGRs caused no acute toxicity on the workers, and any compound had an adverse effect on reproduction (production of males). In addition, larval development was followed in the treated nests compared with the controls. After application of the two MACs and the JHA fenoxycarb no adverse effects were observed on larval development. However, in the nests where the workers were exposed to the JHAs pyriproxyfen and kinoprene higher numbers of dead larvae were scored. These larvae were third and fourth instars, implying a lethal blockage of development before metamorphosis. In a second test, a series of dilutions was made for kinoprene, and these results revealed that only the MFRC caused a toxic effect on the larval development. On the other hand, kinoprene at lower concentrations (0.0650 mg ai/l) had a stimulatory effect on brood production. It was remarkable that ovaries of such treated dominant workers were longer and contained more eggs than in the controls. In a last experiment, the cuticular uptake was determined for a JHA and MAC to evaluate to what extent worker bees accumulate these classes of IGRs. Cuticular uptake ranged from 34 to 83% at 24 h after topical application. Overall, the obtained results indicate that the tested IGRs at their recommended concentration are safe to be used in combination with B. terrestris.

Allergy to bumblebees

Field stings by bumblebees are uncommon because of the habitat and nonaggressiveness of these insects. More stings have been reported in the Netherlands because of the increasing use of bumblebees in flowering industries such as tomato growing. The purpose of this review is to summarize the recent literature concerning bumblebee anaphylaxis and describe our own experience with immunotherapy in an occupational group of bumblebee-venom-allergic workers. Two distinct categories of patients are sensitized to bumblebee venom. First are patients with IgE highly cross-reactive with honeybee venom allergens. Venom immunotherapy with honeybee venom will be adequate in these nonprofessionally exposed bumblebee-allergic patients. These patients react to bumblebee venom as a result of a primary earlier exposure and sensitization to honeybee venom. Secondly, with heavily exposed greenhouse workers or bumblebee workers, frequently stung only by bumblebees, it is recommended to use immunotherapy with purified bumblebee venom, due to the low or absent degree of cross-reactivity with honeybee venom. Otherwise, the best preventive therapy is to avoid further exposure, which means changing profession. Immunotherapy with purified bumblebee venom is as well tolerated and effective as immunotherapy with other Hymenoptera venoms.

Hazards and uptake of chitin synthesis inhibitors in bumblebees Bombus terrestris

This research project examined the potential hazards of a major class of insect growth regulators (IGRs) to survival, reproduction and larval growth in bumblebees Bombus terrestris L. Eight chitin synthesis inhibitors (CSIs) were tested: buprofezin, cyromazine, diflubenzuron, flucycloxuron, flufenoxuron, lufenuron, novaluron and teflubenzuron. These different IGRs, which are important in the control of pest insects in greenhouses, were applied via three different routes of exposure under laboratory conditions: dermal contact, and orally via the drinking of sugar/water and via pollen. The compounds were tested at their respective maximum field recommended concentrations (MFRC) and also in dose-response assays to calculate LC(50) values. In general, none of the CSIs showed acute worker toxicity. However, there was a dramatic reduction in brood production, especially after oral treatment with pollen and sugar/water. Conspicuously, egg fertility was reduced in all treatments with diflubenzuron and teflubenzuron. In addition to egg mortality, the worker bumblebees removed larvae from the treated nest, and in most cases these individuals were dead first-second instars. Under a binocular microscope, such larvae showed an abnormally formed cuticle leading to mechanical weakness and death. In another series of experiments using (14)C-diflubenzuron and (14)C-flufenoxuron, cuticular penetration in workers was studied for a better understanding of the differences in toxicity. With (14)C-diflubenzuron, transovarial transport and accumulation in the deposited eggs supported the strong reproductive effects. Overall, the present results suggest that CSIs should be applied with caution in combination with bumblebees. The compatibility of each compound to be used in combination with B. terrestris is discussed in relation to calculated LC(50) values, routes of uptake and effects.

Insect Immunity Shows Specificity in Protection upon Secondary Pathogen Exposure

Immunological memory in vertebrates, conferring lasting specific protection after an initial pathogen exposure, has implications for a broad spectrum of evolutionary, epidemiological, and medical phenomena . However, the existence of specificity in protection upon secondary pathogen exposure in invertebrates remains controversial . To separate this functional phenomenon from a particular mechanism, we refer to it as specific immune priming. We investigate the presence of specific immune priming in workers of the social insect Bombus terrestris. Using three bacterial pathogens, we test whether a prior homologous pathogen exposure gives a benefit in terms of long-term protection against a later challenge, over and above a heterologous combination. With a reciprocally designed initial and second-exposure protocol (i.e., all combinations of bacteria were tested), we demonstrate, even several weeks after the clearance of a first exposure, increased protection and narrow specificity upon secondary exposure. This demonstrates that the invertebrate immune system is functionally capable of unexpectedly specific and durable induced protection. Ultimately, despite general broad differences between vertebrates and invertebrates, the ability of both immune systems to show specificity in protection suggests that their immune defenses have found comparable solutions to similar selective pressures over evolutionary time.