Bumblebee Workers Research Articles

Aggression or ovarian development as determinants of reproductive dominance in Bombus terrestris: interpretation using a simulation model

Insect societies generally manifest reproductive division of labor with one or a few fecund females (queens) and sterile helpers (workers). This is generally mediated by behavioural hierarchy that reduces the cost of within-group aggression. Aggressive behaviour and ovarian development are thus two co-occurring correlates of reproductive skew, but their mutual influence remains unclear. Here we examined the interplay between these factors by constructing a simulation model, based on the biology of Bombus terrestris, to test whether aggression levels are determined by the level of ovarian development or vice versa. We approached this question using virtual groups composed of either equally or unequally matched workers, as well as supplementing the simulation data by experimental data using actual bee groups. The simulation revealed that previous encounter experience (win/lose) rather than mutual assessment of reproductive status determines and maintains hierarchy in B. terrestris. Furthermore, although bumblebee workers largely vary in their aggression tendencies, pre-existing differences between nest-mates were not obligatory for establishment of the hierarchy. The initially formed linear hierarchy became polynomial after 10 days, clearly separating between egg-laying workers and helpers. This was consistent with the results obtained for actual bee groups. We propose that aggressive behaviour and the outcome of previous encounters are major determinants of ovarian development and not vice versa. Workers may gain a head start in the competition due to variation in their innate aggressive tendencies, or by fortuitously winning their first encounters. Small differences in aggressiveness between workers are amplified to initially form a short-term linear hierarchy that subsequently turns to polynomial hierarchy, creating the most basic phenomenon of social groups, reproductive division of labor.

Wax Lipids Signal Nest Identity in Bumblebee Colonies

The signalling functions of cuticular lipids, particularly cuticular hydrocarbons, have gained considerable attention in social insect communication. Information transfer between individuals by means of these substances has been examined extensively. However, communication with cuticular lipids is not limited to inter-individual recognition. Cuticular compounds can also have a signalling function in the nest environment. Workers of the bumblebee Bombus terrestris leave cuticular lipid traces, so-called footprints, that mark their nest entrance. In addition, there is evidence that bumblebees sense nesting material to identify their colony. In this study, we examined the signalling potential of bumblebee wax, and tested if bumblebee workers are able to identify their colony with the help of wax scent. Chemical analyses of wax extracts using coupled gas chromatography-mass spectrometry showed that wax from colonies of the bumblebee B. terrestris contained a complex blend of cuticular lipids, dominated by hydrocarbons and wax esters. Comparing the relative compound amounts of wax samples from different colonies, we found that wax scent patterns varied with nest identity. Olfactometer bioassays showed that bumblebees were able to discriminate between wax scents from their own and a foreign colony. Our findings suggest that wax emits characteristic olfactory profiles that are used by workers to recognize their colony.

Social Learning in Bumblebees (Bombus impatiens): Worker Bumblebees Learn to Manipulate and Forage at Artificial Flowers by Observation and Communication within the Colony

Social learning occurs when one individual learns from another, mainly conspecific, often by observation, imitation, or communication. Using artificial flowers, we studied social learning by allowing test bumblebees to (a) see dead bumblebees arranged in foraging positions or (b) watch live bumblebees actually foraging or (c) communicate with nestmates within their colony without having seen foraging. Artificial flowers made from 1.5 mL microcentrifuge tubes with closed caps were inserted through the centres of blue 7 cm plastic discs as optical signals through which the bees could not forage. The reinforcer reward syrup was accessible only through holes in the sides of the tubes beneath the blue discs. Two colonies (A and B) were used in tandem along with control (C and D) colonies. No bee that was not exposed (i.e., from the control colonies (C and D)) to social learning discovered the access holes. Inside colony B, we imprisoned a group of bees that were prevented from seeing or watching. Bees that saw dead bumblebees in foraging positions, those that watched nest-mates foraging, and those that had only in-hive communication with successful foragers all foraged successfully. The means of in-hive communication are not understood and warrant intense investigation.

The psychophysics of sugar concentration discrimination and contrast evaluation in bumblebees

The capacity to discriminate between choice options is crucial for a decision-maker to avoid unprofitable options. The physical properties of rewards are presumed to be represented on context-dependent, nonlinear cognitive scales that may systematically influence reward expectation and thus choice behavior. In this study, we investigated the discrimination performance of free-flying bumblebee workers (Bombus impatiens) in a choice between sucrose solutions with different concentrations. We conducted two-alternative free choice experiments on two B. impatiens colonies containing some electronically tagged bumblebees foraging at an array of computer-automated artificial flowers that recorded individual choices. We mimicked natural foraging conditions by allowing uncertainty in the probability of reward delivery while maintaining certainty in reward concentration. We used a Bayesian approach to fit psychometric functions, relating the strength of preference for the higher concentration option to the relative intensity of the presented stimuli. Psychometric analysis was performed on visitation data from individually marked bumblebees and pooled data from unmarked individuals. Bumblebees preferred the more concentrated sugar solutions at high stimulus intensities and showed no preference at low stimulus intensities. The obtained psychometric function is consistent with reward evaluation based on perceived concentration contrast between choices. We found no evidence that bumblebees reduce reward expectations upon experiencing non-rewarded visits. We compare psychometric function parameters between the bumblebee B. impatiens and the flower bat Glossophaga commissarisi and discuss the relevance of psychophysics for pollinator-exerted selection pressures on plants.

Behavioural plasticity in the fanning response of bumblebee workers: impact of experience and rate of temperature change

Flexible division of labour is a key feature of social insects. Our understanding of individual response behaviour and how it is integrated into a functioning colony is still patchy. Most theoretical studies addressing this question are based on the assumption that workers have intrinsic and often fixed response thresholds for task-related stimuli. Here, we investigated the plasticity in worker fanning response behaviour in a bumblebee, Bombus terrestris. Using a temperature-controlled brood dummy, we first asked whether the fanning response is modulated by rate of temperature change. Second, we examined to what extent the fanning response is influenced by recent fanning experience. Our results show that the individual fanning response is modulated by both the rate of temperature increase and recent experience. Workers responded at lower temperatures and with a higher probability when the temperature of the brood dummy increased slowly compared with more rapid temperature increases. Workers that repeatedly responded to an increase in brood dummy temperature with fanning showed a significant decrease in their response thresholds, whereas the response thresholds of control workers that experienced the same treatment but did not gather fanning experience remained unchanged. The decrease in response threshold was pronounced when the time interval between two successive fanning events was less than 6 h. When 16 h or more separated fanning events, individual fanning responses returned to higher threshold levels. We suggest that experience-dependent modulation of response thresholds plays an important role in the behavioural differentiation of workers and the flexibility of insect colonies.

Bumblebees and pesticides

A study showing the effects of two pesticides on bumblebees highlights the need for risk assessments to consider multiple species and the complex chain of factors that determines insect exposure to chemicals. See Letter p.105 Exposure to neonicotinoid pesticides is known to influence bee behaviour, and could be a key factor in current bee declines. It has not been possible to establish a mechanistic link between individual and colony effects, but this study demonstrates a direct link between detrimental behavioural effects and field-level pesticide exposure — to neonicotinoid and pyrethroid — in individual worker bumblebees, and consequent impacts on colony development and survival. The pesticides reduce the effectiveness of foraging behaviour, with knock-on effects on brood care and colony productivity.

Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid)

Currently, there is concern about declining bee populations and the sustainability of pollination services. One potential threat to bees is the unintended impact of systemic insecticides, which are ingested by bees in the nectar and pollen from flowers of treated crops. To establish whether imidacloprid, a systemic neonicotinoid and insect neurotoxin, harms individual bees when ingested at environmentally realistic levels, we exposed adult worker bumble bees, Bombus terrestris L. (Hymenoptera: Apidae), and honey bees, Apis mellifera L. (Hymenoptera: Apidae), to dietary imidacloprid in feeder syrup at dosages between 0.08 and 125μgl−1. Honey bees showed no response to dietary imidacloprid on any variable that we measured (feeding, locomotion and longevity). In contrast, bumble bees progressively developed over time a dose-dependent reduction in feeding rate with declines of 10–30% in the environmentally relevant range of up to 10μgl−1, but neither their locomotory activity nor longevity varied with diet. To explain their differential sensitivity, we speculate that honey bees are better pre-adapted than bumble bees to feed on nectars containing synthetic alkaloids, such as imidacloprid, by virtue of their ancestral adaptation to tropical nectars in which natural alkaloids are prevalent. We emphasise that our study does not suggest that honey bee colonies are invulnerable to dietary imidacloprid under field conditions, but our findings do raise new concern about the impact of agricultural neonicotinoids on wild bumble bee populations.

On the relationship between aggression and reproduction in pairs of orphaned worker bumblebees (Bombus impatiens)

This study characterized aggression and reproduction within pairs of orphaned bumblebee sisters (Bombus impatiens (Cresson, 1863)). Twenty-one pairs were filmed in the laboratory over 5–10 days. Frequencies of aggression and egg-laying were obtained for each bee, and the presence or absence of brood was manipulated. Aggression and egg-laying were more likely to co-occur in pairs placed without brood compared to pairs placed with brood. A significant positive correlation was found between members of a pair in the rates of aggression. In addition, a strong positive correlation was found in their rates of egg-laying: bees that had more sons also tended to have more nephews. The results show that under conditions of unrestricted food availability, behavioural interactions are compatible with continued reproduction by both orphaned workers. Though aggression may limit reproduction, it seems either to be an ineffective means of obtaining a reproductive monopoly in some situations and/or to be a set of behaviours invested with other possible functions.

Bumble Bee (Hymenoptera: Apidae) Foraging Distance and Colony Density Associated With a Late-Season Mass Flowering Crop

ABSTRACT Foraging behaviors of bumble bee workers have been examined in natural habitats, whereas agricultural landscapes, which can provide insights on flight distances to fragmented patches of bloom, have received limited attention. In particular, information on worker flight distances to crops blooming several months after nests have been established is invaluable. Here, we examined foraging patterns of Bombus vosnesenskii Radoszkowski in late-season blooming clover in the agriculturaldominated Willamette Valley in Oregon. Workers from 10 fields collected over 2 yr were assigned to full sibling families (colonies) by using eight microsatellite loci. With estimation of numbers of unseen species, we inferred the presence of 189 colonies from 433 bees genotyped in year 1, and 144 from 296 genotyped the next year. Worker foraging distance was estimated to be at least 11.6 km, half the distance between the most remote fields visited by the same colonies. Numbers of nests contributing workers to each field r...

Erratum to: Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris)

Erratum to: Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris)

Ecological effects on gut bacterial communities in wild bumblebee colonies

1. Animal hosts harbour diverse and often specific bacterial communities (microbiota) in their gut. These microbiota can provide crucial services to the host such as aiding in digestion of food and immune defence. However, the ecological factors correlating with and eventually shaping these microbiota under natural conditions are poorly understood. 2. Bumblebees have recently been shown to possess simple and highly specific microbiota. We here examine the dynamics of these microbiota in field colonies of the bumblebee Bombus terrestris over one season. The gut bacteria were assessed with culture-independent methods, that is, with terminal restriction fragment length profiles of the 16S rRNA gene. 3. To further understand the factors that affect the microbiota, we experimentally manipulated field-placed colonies in a fully factorial experiment by providing additional food or by priming the workers' immune system by injecting heat-killed bacteria. We furthermore looked at possible correlates of diversity and composition of the microbiota for (i) natural infections with the microbial parasites Crithidia bombi and Nosema bombi, (ii) bumblebee worker size, (iii) colony identity, and (iv) colony age. 4. We found an increase in diversity of the microbiota in individuals naturally infected with either C. bombi or N. bombi. Crithidia bombi infections, however, appear to be only indirectly linked with higher microbial diversity when comparing colonies. The treatments of priming the immune system with heat-killed bacteria and additional food supply, as well as host body size, had no effect on the diversity or composition of the microbiota. Host colony identity had only a weak effect on the composition of the microbiota at the level of resolution of our method. We found both significant increases and decreases in the relative abundance of selected bacterial taxa over the season. 5. We present the first study on the ecological dynamics of gut microbiota in bumblebees and identify parasite infections, colony identity and colony age as important factors influencing the diversity and composition of the bacterial communities. The absence of an effect of our otherwise effective experimental treatments suggests a remarkable ability of the host to maintain a homoeostasis in this community under widely different environments.

Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris)

Bumble bees are important pollinators whose populations have declined over recent years, raising widespread concern. One conspicuous threat to bumble bees is their unintended exposure to trace residues of systemic neonicotinoid pesticides, such as imidacloprid, which are ingested when bees forage on the nectar and pollen of treated crops. However, the demographic consequences for bumble bees of exposure to dietary neonicotinoids have yet to be fully established. To determine whether environmentally realistic levels of imidacloprid are capable of making a demographic impact on bumble bees, we exposed queenless microcolonies of worker bumble bees, Bombus terrestris, to a range of dosages of dietary imidacloprid between zero and 125 μg L(-1) and examined the effects on ovary development and fecundity. Microcolonies showed a dose-dependent decline in fecundity, with environmentally realistic dosages in the range of 1 μg L(-1) capable of reducing brood production by one third. In contrast, ovary development was unimpaired by dietary imidacloprid except at the highest dosage. Imidacloprid reduced feeding on both syrup and pollen but, after controlling statistically for dosage, microcolonies that consumed more syrup and pollen produced more brood. We therefore speculate that the detrimental effects of imidacloprid on fecundity emerge principally from nutrient limitation imposed by the failure of individuals to feed. Our findings raise concern about the impact of neonicotinoids on wild bumble bee populations. However, we recognize that to fully evaluate impacts on wild colonies it will be necessary to establish the effect of dietary neonicotinoids on the fecundity of bumble bee queens.

Size‐related variation in protein abundance in the brain and abdominal tissue of bumble bee workers

Female bumble bee workers of the same species often show a profound body size variation that is linked to a division of labour. Large individuals are more likely to forage whereas small individuals are more likely to perform in-nest activities. A higher sensory sensitivity, stronger circadian rhythms as well as better learning and memory performances appear to better equip large individuals for outdoor activities compared to their smaller siblings. The molecular mechanisms underlying worker functional polymorphism remain unclear. Proteins are major determinants of an individual's morphology and behaviour. We hypothesized that the abundance of proteins such as metabolic enzymes as well as proteins involved in neuronal functions would differ with body size and provide insights into the mechanisms underlying size-dependent physiological specialization in bumble bee workers. We conducted protein quantification measurements based on liquid chromatography coupled with tandem mass spectrometry on tissue samples derived from small and large Bombus impatiens and Bombus terrestris workers. Proteins found to differ significantly in abundance between small and large workers belong to the categories of structure, energy metabolism and stress response. These findings provide the first proteomic insight into mechanisms associated with size-based division of labour in social insects.

Morphological and Physiological Idiosyncrasies Lead to Interindividual Variation in Flight Metabolic Rate in Worker Bumblebees (Bombus impatiens)

Although intraspecific variation in metabolic rate is associated with variation in body size, similarly sized individuals nonetheless vary greatly. At similar masses, hovering bumblebee workers (Bombus impatiens) can differ in metabolic rate up to twofold. We examined how such interindividual variation arises by studying covariation of flight metabolic rate with morphological and other physiological parameters. Body size alone explained roughly half the variation in flight metabolic rate. The remaining variation could be explained as the outcome of variation in wing morphology and possibly an association with variation in flight muscle metabolic enzyme activities. As shown using statistical models, for a given mass, higher metabolic rate was correlated with both higher thoracic temperature and higher wing stroke frequency, in turn resulting from smaller wing surface area. When organismal and cellular metabolism for a given mass were linked, variation in metabolic rate was positively correlated with the activities of trehalase and hexokinase. Altogether, covariation with morphology and other physiological parameters explains up to 75% of the variation in metabolic rate. We also investigated the role of flight experience and show that neither flight restriction nor the number of lifetime flights affected flight energetics or flight muscle phenotype. Additionally, manipulating the level of wing asymmetry increased flight wing stroke frequency, metabolic rate, and thoracic temperature, but it did not alter enzyme activity. We conclude that idiosyncrasies in body morphology largely explained interindividual variation in flight metabolic rate but flight muscle metabolic phenotype shows little variation associated with differences in flight experience.

Social context-dependent immune gene expression in bumblebees (Bombus terrestris)

Social insects are prone to attack by parasites as they provide numerous resources of food and brood, homeostatic nest conditions and a high density of individuals, enhancing the transmission of parasites. The defence of social insects might occur at different levels, the individual and the group. Individual defence occurs in part via the innate immune system resulting in the expression of antimicrobial substances. Group level defences, summarised as ‘social immunity’, represent a suite of behavioural and organisational features. Here, all effects contributing to social immunity except for the social context were removed from bumblebee (Bombus terrestris) workers, kept either in groups or solitarily. The gene expression of six effector molecules of the immune system was monitored in both groups and in controls from the same source colonies. The social treatment has a highly significant effect on immune gene expression, with groups exhibiting higher levels of two antimicrobial peptides (AMPs) and two lysozymes. Phenoloxidase is affected at the regulatory level, with a strong upregulation of its suppressor Spn27A in groups suggesting a trade-off with antimicrobial activity. AMPs are strongly upregulated in groups, whereas lysozymes are strongly downregulated in solitary treatments suggesting another trade-off. Clearly, social immunity impacts elements of individual immunity.

Effects of Soil Quality Enhancement on Pollinator-Plant Interactions

Both biotic and abiotic factors can affect soil quality, which can significantly impact plant growth, productivity, and resistance to pests. However, the effects of soil quality on the interactions of plants with beneficial arthropods, such as pollinators, have not been extensively examined. We studied the effects of vermicompost (earthworm compost, VC) soil amendment on behavioral and physiological responses of pollinators to flowers and floral resources, using cucumbers,Cucumis sativus, as our model system. Results from experiments conducted over three field seasons demonstrated that, in at least two out of three years, VC amendment significantly increased visit length, while reducing the time to first discovery. Bumblebee (Bombus impatiens) workers that fed on flowers from VC-amended plants had significantly larger and more active ovaries, a measure of nutritional quality. Pollen fractions of flowers from VC-grown plants had higher protein compared to those of plants grown in chemically fertilized potting soil. Nectar sugar content also tended to be higher in flowers from VC-grown plants, but differences were not statistically significant. In conclusion, soil quality enhancement, as achieved with VC amendment in this study, can significantly affect plant-pollinator interactions and directly influences pollinator nutrition and overall performance.

Species Diversity of Bumblebees (Hymenoptera: Apidae) from Different Mountain Regions of Kashmir Himalayas

The species diversity of bumblebees was investigated in three provinces Jammu, Kashmir and Ladakh during 2007-2010. Bumblebee queens, workers and males were collected right from the commencement till to the end of flowering stage in all the three mountain regions. In total, 27 species of bumblebees were collected and identified, of which eleven species were common in the two regions, e.g., Kashmir and Ladakh. A list of species assemblages and abundance is provided in each of the mountain ranges. Species diversity of three regions was determined with Shannon-Weiner diversity index and evenness was calculated with indices of Pielou. The obtained results showed species diversity; evenness and species richness were more observable in Kashmir compared with Ladakh and Jammu. The three sample sites within the Kashmir Himalayas indicate significant differences in species diversity; the Kashmir region had higher species diversity and richness than the other regions. Most species of bumblebees were collected in altitudinal ranges of 3000-4000m. Four species viz. Bombus cornutus, B. parthenius, B. miniatus and B. morawitizianus are recorded for the first time from this region, while B. morawitizianus turn out to be the first record to the national list.Key words: Species Diversity; Bumblebees; Kashmir Himalayas.© 2012 JSR Publications. ISSN: 2070-0237 (Print); 2070-0245 (Online). All rights reserved.doi: http://dx.doi.org/10.3329/jsr.v4i1.8815J. Sci. Res. 4 (1), 263-272 (2012)

The benefits of being sociable

Social species of honey bees and bumble bees carry in their gut a species-poor bacterial community that is absent from solitary bee species. To examine the role of this gut microbiota, the authors raised worker bumble bees in a semisterile environment when they emerged from the pupae, and fed them either faeces from their nest mates or sterile sugar water (controls). Following inoculation with the parasite Crithidia bombi, controls (which lacked a normal gut microbiota) showed significantly higher levels of infection and parasite numbers than the faeces-fed workers. Similarly, wild-caught bees were less likely to be infected with this parasite if they carried a normal gut microbiota. Solitary bees are known to lack this gut microbiota, so the authors propose that the social environment facilitates the transmission of commensals between nest mates during gut formation, which may then protect the bees from parasites through competition for resources or secretion of antimicrobials.

Percent lipid is associated with body size but not task in the bumble bee Bombus impatiens

In some group-living organisms, labor is divided among individuals. This allocation to particular tasks is frequently stable and predicted by individual physiology. Social insects are excellent model organisms in which to investigate the interplay between physiology and individual behavior, as division of labor is an important feature within colonies, and individual physiology varies among the highly related individuals of the colony. Previous studies have investigated what factors are important in determining how likely an individual is, compared to nestmates, to perform certain tasks. One such task is foraging. Corpulence (i.e., percent lipid) has been shown to determine foraging propensity in honey bees and ants, with leaner individuals being more likely to be foragers. Is this a general trend across all social insects? Here we report data analyzing the individual physiology, specifically the percent lipid, of worker bumble bees (Bombus impatiens) from whom we also analyze behavioral task data. Bumble bees are also unusual among the social bees in that workers may vary widely in size. Surprisingly we find that, unlike other social insects, percent lipid is not associated with task propensity. Rather, body size closely predicts individual relative lipid stores, with smaller worker bees being allometrically fatter than larger worker bees.

Bombus terrestris as pollinator‐and‐vector to suppress Botrytis cinerea in greenhouse strawberry

Bombus terrestris L. bumblebees are widely used as commercial pollinators, but they might also be of help in the battle against economically important crop diseases. This alternative control strategy is referred to as pollinator-and-vector technology. The present study was designed to investigate the capacity of B. terrestris to fulfil this role in greenhouse strawberry flowers, which were manually inoculated with a major plant pathogen, the grey mould Botrytis cinerea Pers.: Fr. A model microbiological control agent (MCA) product Prestop-Mix was loaded in a newly developed two-way bumblebee dispenser, and, in addition, the use of the diluent Maizena-Plus (corn starch) was tested. Importantly, loading of the MCA caused no adverse effects on bumblebee workers, with no loss of survival or impairment of flight activity of the workers during the 4 week flowering period. Secondly, vectoring of Prestop-Mix by bumblebees resulted in a higher crop production, as 71% of the flowers developed into healthy red strawberries at picking (preharvest yield) as compared with 54% in the controls. In addition, these strawberries were better protected, as 79% of the picked berries remained free of B. cinerea after a 2 day incubation (post-harvest yield), while this percentage was only 43% in the control. Overall, the total yield (preharvest × post-harvest) was 2-2.5 times higher than the total yield in the controls (24%) in plants exposed to bumblebees vectoring Prestop-Mix. Thirdly, the addition of the diluent Maizena-Plus to Prestop-Mix at 1:1 (w/w) resulted in a similar yield to that of Prestop-Mix used alone, and in no negative effects on the bumblebees, flowers and berries. This greenhouse study provides strong evidence that B. terrestris bumblebees can vector a MCA to reduce B. cinerea incidence in greenhouse strawberries, resulting in higher yields. Similar yields obtained in the treatments with Prestop-Mix and Prestop-Mix + Maizena-Plus suggest an equally efficient dissemination of the biocontrol agent into the flowers with only half the initial concentration of Prestop-Mix, which illustrates the importance of the diluent.