Ontogeny of worker body size distribution in bumble bee (Bombus impatiens) colonies

1. Bumble bees exhibit worker size polymorphisms; highly related workers within a colony may vary up to 10‐fold in body mass. As size variation is an important life history feature in bumble bees, the distribution of body sizes within the colony and how it fluctuates over the colony cycle were analysed. 2. Ten commercially purchased colonies of Bombus impatiens (Cresson) were reared in ad libitum conditions. The size of all workers present and newly emerging workers (callows) was recorded each week. 3. The average size of bumble bee workers did not change with colony age, but variation in body size tended to decrease over time. The average size of callows did not change with population size, but did tend to decrease with colony age. In all measures, there was considerable variation among colonies. 4. Colonies of B. impatiens usually produced workers with normally distributed body sizes throughout the colony life cycle. Unlike most polymorphic ants, there was no increase in worker body size with colony age or colony size. This provides the first, quantitative data on the ontogeny of bumble bee worker size distribution. The potential adaptive significance of this size variation is discussed.     

The power and efficiency of brood incubation in queenless microcolonies of bumble bees (Bombus terrestris L.)

1. Ground‐nesting colonies of bumble bees incubate their brood at > 30 °C if floral forage provides sufficient energy and the thermogenic power of the colony can counteract cool soil conditions. To explore the basis of incubation, the thermogenic power and sugar consumption of orphaned nests of bumble bee workers (microcolonies) were investigated under laboratory conditions. 2. This study tested experimentally the effect of variation in worker number (ranging from four to 12 adults) on a microcolony's capacity to regulate brood temperature and recover from acute cold exposure. Microcolonies were provided with ad libitum sugar syrup and minimal insulation and maintained at an ambient temperature of c. 25 °C. Energy conversion efficiency was estimated by comparing sugar consumption with the power required for artificial incubation. The joint energetics of foraging and incubation were modelled in wild colonies to explore the effect of colony size and landscape quality on thermoregulation. 3. The results showed that all sizes of microcolonies regulated brood temperature at c. 31 °C under laboratory conditions, which required 96 mW of thermogenic power. It was estimated that individual workers of B. terrestris generated an incubatory power of 35 mW. The smallest microcolonies had the highest conversion efficiency (57%), apparently because few workers were required for incubation. 4. Modelling indicated that small microcolonies of three to seven adult workers have the capacity for normal brood incubation in the wild, but that the minimum viable colony size increases as floral forage becomes poorer or more distant. 5. These preliminary findings suggest the feasibility of identifying the minimum conditions (forage quality, soil temperature, and colony size) necessary for brood incubation by queenright colonies in the wild.     

Spatial ecology of a range‐expanding bumble bee pollinator

Molecular methods have greatly increased our understanding of the previously cryptic spatial ecology of bumble bees (Bombus spp.), with knowledge of the spatial ecology of these bees being central to conserving their essential pollination services. Bombus hypnorum, the Tree Bumble Bee, is unusual in that it has recently rapidly expanded its range, having colonized much of the UK mainland since 2001. However, the spatial ecology of B. hypnorum has not previously been investigated. To address this issue, and to investigate whether specific features of the spatial ecology of B. hypnorum are associated with its rapid range expansion, we used 14 microsatellite markers to estimate worker foraging distance, nest density, between‐year lineage survival rate and isolation by distance in a representative UK B. hypnorum population. After assigning workers to colonies based on full or half sibship, we estimated the mean colony‐specific worker foraging distance as 103.6 m, considerably less than values reported from most other bumble bee populations. Estimated nest density was notably high (2.56 and 0.72 colonies ha^?1 in 2014 and 2015, respectively), estimated between‐year lineage survival rate was 0.07, and there was no evidence of fine‐scale isolation by distance. In addition, genotyping stored sperm dissected from sampled queens confirmed polyandry in this population (mean minimum mating frequency of 1.7 males per queen). Overall, our findings establish critical spatial ecological parameters and the mating system of this unusual bumble bee population and suggest that short worker foraging distances and high nest densities are associated with its rapid range expansion.     

Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites

Abstract.

• 1 In natural populations, colonies of bumble bees vary in many important life history traits, such as colony size and age at maturity, or the number and sex of reproductives produced. We investigated how the presence of parasites in field populations of the bumble bee Bombus lucorum L. relates to variation in life history traits and reproductive performance. A total of thirty-six colonies was placed in accessible nest sites in the field and monitored at regular intervals throughout a season.
• 2 Among the life history correlates, early nest foundation was strongly associated with large maximum colony size, old age and large size at maturity, and this in turn with successful production of males and queens, as well as with the number of sexuals produced. Overall, reproductive success was highly skewed with only five colonies producing all the queens. Sixteen colonies failed to reproduce altogether.
• 3 The social parasite Psithyrus was abundant early in the Bombus colony cycle and preferentially invaded host nests with many first brood workers and thus disproportionately large size, i.e. those colonies that would otherwise be more likely to reproduce or produce (daughter) queens rather than males. To prevent nest loss, Psithyrus had to be removed soon after invasion. Therefore, the effects reported here can only be crude estimates.
• 4 Parasitoid conopid flies are likely to cause heavy worker mortality when sexuals are reared by the colonies. Their inferred effect was a reduction in biomass that could be invested in sexuals as well as a shift in the sex ratio at the population level resulting from failure to produce queens. We suggest to group the inferred correlates into ‘early events’ surrounding colony initiation and social parasitism, and ‘late events’ surrounding attained colony size in summer and parasitism by conopid flies. Our evidence thus provides a heuristic approach to understand the factors that affect reproductive success of Bombus colonies.

     

The relationship between the distribution of worker sizes and new worker production in the ant Formica neorufibarbis

While it is commonly assumed that variation in worker sizes within a single ant colony increases colony efficiency, there is little causal evidence of a link between worker size variation and colony performance. I tested whether the range of worker sizes within colonies of the ant species Formica neorufibarbis affected new worker production. Removing large workers from colonies lowered the rate of new worker production. A study of unmanipulated colonies indicated that colonies did not maintain a full range of worker sizes; mean worker head widths varied from 0.89-1.24 mm. Colonies naturally missing large workers did not have lower rates of worker production, suggesting that the relative size, not the absolute size, of workers within colonies was important. These are the first results to directly link the range of worker sizes to a component of colony fitness in a natural setting.     

Foraging errors play a role in resource exploration by bumble bees (Bombus terrrestris)

If the cognitive performance of animals reflects their particular ecological requirements, how can we explain appreciable variation in learning ability amongst closely related individuals (e.g. foraging workers within a bumble bee colony)? One possibility is that apparent ‘errors’ in a learning task actually represent an alternative foraging strategy. In this study we investigate the potential relationship between foraging ‘errors’ and foraging success among bumble bee (Bombus terrestris) workers. Individual foragers were trained to choose yellow, rewarded flowers and ignore blue, unrewarded flowers. We recorded the number of errors (visits to unrewarded flowers) each bee made during training, then tested them to determine how quickly they discovered a more profitable food source (either familiar blue flowers, or novel green flowers). We found that error prone bees discovered the novel food source significantly faster than accurate bees. Furthermore, we demonstrate that the time taken to discover the novel, more profitable, food source is positively correlated with foraging success. These results suggest that foraging errors are part of an ‘exploration’ foraging strategy, which could be advantageous in changeable foraging environments. This could explain the observed variation in learning performance amongst foragers within social insect colonies.     

Non-lethal sampling of DNA from bumble bees for conservation genetics

Summary Non-lethal sampling of DNA from individuals in wild populations will often be required for studies of the conservation genetics of social insects, since it avoids destroying members of scarce or declining species. We investigated the effectiveness and consequences of methods of non-lethal sampling of DNA from bumble bee workers. In an experiment with two captive and confined Bombus terrestris colonies, we found that, unlike sampling haemolymph, sampling the terminal portion of the tarsus of a mid-leg of a worker reliably yielded amplifiable microsatellite DNA and did not significantly reduce worker survivorship. In a further experiment with four B. terrestris colonies whose workers were allowed to forage freely at flowers in the external environment, tarsal sampling of either a mid-leg or a hind-leg had no significant effects on worker survivorship, the mean body mass of foraging workers, the frequency or duration of foraging trips, mass of pollen loads or mass of nectar loads. We therefore suggest that tarsal sampling of either a mid-leg or a hind-leg is an effective and acceptable means of non-lethally sampling DNA from workers in wild populations of bumble bees, because effects on individual and colony performance are likely to be absent or minimal.Received 2 December 2002; revised 10 April 2003; accepted 25 April 2003.     

Fine‐scale spatial genetic structure of common and declining bumble bees across an agricultural landscape

Land‐use changes have threatened populations of many insect pollinators, including bumble bees. Patterns of dispersal and gene flow are key determinants of species' ability to respond to land‐use change, but have been little investigated at a fine scale (<10 km) in bumble bees. Using microsatellite markers, we determined the fine‐scale spatial genetic structure of populations of four common Bombus species (B. terrestris, B. lapidarius, B. pascuorum and B. hortorum) and one declining species (B. ruderatus) in an agricultural landscape in Southern England, UK. The study landscape contained sown flower patches representing agri‐environment options for pollinators. We found that, as expected, the B. ruderatus population was characterized by relatively low heterozygosity, number of alleles and colony density. Across all species, inbreeding was absent or present but weak (F_IS = 0.01–0.02). Using queen genotypes reconstructed from worker sibships and colony locations estimated from the positions of workers within these sibships, we found that significant isolation by distance was absent in B. lapidarius, B. hortorum and B. ruderatus. In B. terrestris and B. pascuorum, it was present but weak; for example, in these two species, expected relatedness of queens founding colonies 1 m apart was 0.02. These results show that bumble bee populations exhibit low levels of spatial genetic structure at fine spatial scales, most likely because of ongoing gene flow via widespread queen dispersal. In addition, the results demonstrate the potential for agri‐environment scheme conservation measures to facilitate fine‐scale gene flow by creating a more even distribution of suitable habitats across landscapes.     

Improvement of almond production using Bombus terrestris (Hymenoptera: Apidae) in Mediterranean conditions

Almond trees are one of the most important crops in the Balearic Islands. The pollination of almonds is limited to the activity of insects, and cross‐pollination is necessary for fruit development. Currently, honey bees and wild bee populations are declining considerably due to multiple causes, such as the use of pesticides, diseases and habitat loss. An alternative to increase the almond production is the use of commercial pollinators. In this long‐term (3 years) study, the effect of the introduction of Bombus terrestris colonies on almond production was evaluated in two orchards. Two experimental designs were carried out to study the best management of this pollinator. For 2 years, all bumble bee colonies were placed in the middle of the plot and during the last year, the bumble bee colonies were distributed homogenously in the plot. Fruit set and the foraging behaviour of bumble bees during the blossoming period was determined, and the effect of different environmental variables on the visitation rate of bumble bees was assessed by means of a generalized linear mixed model (GLMM). Moreover, for the first time, the spatial distribution of fruit set was evaluated. Our results show that fruit set was significantly higher in the fields where B. terrestris had been introduced than in the control plots. This increased production resulted in a positive economic balance for the farmer. Moreover, bumble bees showed to prefer trees in a southwest orientation that were close to their colony. The activity of bumble bees showed to be significantly influenced by wind speed (the higher the speed the more flowers are visited by B. terrestris) and time after flowering (visitation rate decreased with days after flowering). In order to improve its management and obtain the highest possible almond production, it is important to understand the activity and behaviour of this pollinator.     

Reduced abundance and earlier collection of bumble bee workers under intensive cultivation of a mass‐flowering prairie crop

One of the most commonly seeded crops in Canada is canola, a cultivar of oilseed rape (Brassica napus). As a mass‐flowering crop grown intensively throughout the Canadian Prairies, canola has the potential to influence pollinator success across tens of thousands of square kilometers of cropland. Bumble bees (Bombus sp.) are efficient pollinators of many types of native and crop plants. We measured the influence of this mass‐flowering crop on the abundance and phenology of bumble bees, and on another species of social bee (a sweat bee; Halictus rubicundus), by continuously deploying traps at different levels of canola cultivation intensity, spanning the start and end of canola bloom. Queen bumble bees were more abundant in areas with more canola cover, indicating that this crop is attractive to queens. However, bumble bee workers were significantly fewer in these locations later in the season, suggesting reduced colony success. The median collection dates of workers of three bumble bee species were earlier near canola fields, suggesting a dynamic response of colonies to the increased floral resources. Different species experienced this shift to different extents. The sweat bee was not affected by canola cultivation intensity. Our findings suggest that mass‐flowering crops such as canola are attractive to bumble bee queens and therefore may lead to higher rates of colony establishment, but also that colonies established near this crop may be less successful. We propose that the effect on bumble bees can be mitigated by spacing the crop more evenly with respect to alternate floral resources.     

Effects of within‐colony competition on body size asymmetries and reproductive skew in a social spider

Reproductive partitioning is a key component of social organization in groups of cooperative organisms. In colonies of permanently social spiders of the genus Stegodyphus less than half of the females reproduce, while all females, including nonreproducers, perform suicidal allo‐maternal care. Some theoretical models suggest that reproductive skew is a result of contest competition within colonies, leading to size hierarchies where only the largest females become reproducers. We investigated the effect of competition on within‐group body size variation over six months in S. dumicola, by manipulating food level and colony size. We found no evidence that competition leads to increased size asymmetry within colonies, suggesting that contest competition may not be the proximate explanation for reproductive skew. Within‐colony body size variation was high already in the juvenile stage, and did not increase over the course of the experiment, suggesting that body size variation is shaped at an early stage. This might facilitate task specialization within colonies and ensure colony‐level reproductive output by early allocation of reproductive roles. We suggest that reproductive skew in social spiders may be an adaptation to sociality selected through inclusive fitness benefits of allo‐maternal care as well as colony‐level benefits maximizing colony survival and production.     

Honey bee waggle dance communication increases diversity of pollen diets in intensively managed agricultural landscapes

The benefits of honey bee dance communication for colony performance in different resource environments are still not well understood. Here, we test the hypothesis that directional dance communication enables honey bee colonies to maintain a diverse pollen diet, especially in landscapes with low resource diversity. To test this hypothesis, we placed 24 Apis mellifera L. colonies with either intact or experimentally disrupted dance communication in eight agricultural landscapes that differed in the diversity of flowering plants and in the dominance of mass‐flowering crops. Pollen from incoming foragers was collected and identified via DNA metabarcoding. Disrupting dance communication affected the way the diversity of honey bee pollen diets was impacted by the dominance of mass‐flowering crops in available flower resources (p = .04). With increasing dominance of mass‐flowering crops in resource environments, foragers of colonies with intact communication foraged on an increasing proportion of available plant genera (p = .01). This was not the case for colonies with disrupted dance communication (p = .5). We conclude that the honey bee dance communication benefits pollen foraging on diverse plant resources and thereby contributes to high quality nutrition in environments with low‐resource diversity.     

Geographical and individual variation in echolocation calls of the intermediate leaf‐nosed bat,Hipposideros larvatus

The cause and significance of variation in echolocation call frequency within hipposiderid bats is not well understood despite an increasing number of allopatric and sympatric examples being documented. We examined variation patterns in the resting frequency (RF) of echolocation calls emitted by the intermediate leaf‐nosed bat, Hipposideros larvatus, on a broad geographical scale. Data mining technology and Kruskal–Wallis test both showed substantial variation with a longitudinal pattern in RF in H. larvatus among colonies, and this variation was associated with geographical distance and not body size. In addition, we found that a high degree of variability between individuals was hidden under the geographical variation. The results support an effect of random cultural drift, and challenge the prey detection hypothesis. Moreover, an acoustic difference among local island colonies may be indicative of a vocal dialect. We found that each colony of H. larvatus seems to maintain a ‘private bandwidth’, which could be used for colony identity and individual communication thus helping individuals and colonies to get a number of fitness benefits.     

Effects of social conditions on Juvenile Hormone mediated reproductive development in Bombus terrestris workers

Abstract. During the annual life cycle of the bumble bee Bombus terrestris (L.) colony, there is a stage characterized by worker reproduction in the presence of the queen. It has been proposed that this is a result of a decrease in queen inhibition. This hypothesis was examined by studying the effects of queens taken from colonies at different stages of development on several aspects of worker physiology and behaviour: rates of Juvenile Hormone (JH) release in vitro , ovary development, and behaviour associated with reproduction. After optimizing and validating the radiochemical assay for JH release for bumble bee workers, we found that queenless workers had significantly more developed ovaries and higher rates of release of JH than did queenright workers, confirming and extending previous findings that suggest that bumblebee ovarian development is under JH control. Mated queens, separated from their colony and brood, can have the same inhibitory effect on the reproductive development of callow workers. In contrast, workers confined with virgin queens or in queenless groups demonstrated a significantly higher rate of release of JH, overt aggression and threatening behaviours. However, there were no differences in rates of release of JH between workers confined in groups in the laboratory with queens taken from colonies either before or after the onset of worker reproduction. Furthermore, overt aggression and threatening behaviours were similar and low in both types of groups. These results gave no support to the hypothesis that a decrease in queen inhibition is associated with the onset of worker reproduction. We also show that young workers reared in colonies either before or after worker reproduction occurs, or in queenless colonies, all demonstrated similar, low rates of release of JH. These results suggest that older workers may inhibit the corpora allata of younger workers in queenless colonies.     

Effects of clothianidin on Bombus impatiens (Hymenoptera: Apidae) colony health and foraging ability

We conducted laboratory experiments to investigate the lethal and sublethal effects of clothianidin on bumble bee, Bombus impatiens Cresson, colony health and foraging ability. Bumble bee colonies were exposed to 6 ppb clothianidin, representing the highest residue levels found in field studies on pollen, and a higher dose of 36 ppb clothianidin in pollen. Clothianidin did not effect pollen consumption, newly emerged worker weights, amount of brood or the number of workers, males, and queens at either dose. The foraging ability of worker bees tested on an artificial array of complex flowers also did not differ among treatments. These results suggest that clothianidin residues found in seed-treated canola and possibly other crops will not adversely affect the health of bumble bee colonies or the foraging ability of workers.     

Behavioral responses of the small hive beetle,Aethina tumida,to odors of three meliponine bee species and honey bees,Apis mellifera scutellata

Recent studies have shown that honey bees, bumble bees, and some meliponine bee species of the genera Trigona, Meliponula, and Dactylurina are hosts of the small hive beetle (SHB) Aethina tumidaMurray (Coleoptera: Nitidulidae), a pest of honey bee colonies in various regions of the world. Olfaction has been implicated in SHB infestations of honey bee and bumble bee colonies. We used olfactometer bioassays to investigate responses of adult male and female SHBs to odors from intact colonies and separate hive components (pot honey, pot pollen, cerumen, and propolis) of three African meliponine bee species, Meliponula ferruginea (Lepeletier) (black morphospecies), M. ferruginea (reddish brown morphospecies), and Meliponula bocandei (Spinola) (Hymenoptera: Apidae). Although both sexes of the beetle strongly preferred intact colony, pot honey, and pot pollen odors, there was no evidence of attraction to propolis and cerumen odors from the three meliponine bee species. Both sexes of SHB also strongly preferred odors from honey bees, Apis mellifera L. (Hymenoptera: Apidae), over odors from the three meliponine bee species. Our results provide substantial evidence of the host potential of African meliponine bees for the SHB, and we discuss this complex association of the SHB with species within the Apidae family.     

Small worker bumble bees (Bombus impatiens) are hardier against starvation than their larger sisters

In bumble bees (Bombus spp.), where workers within the same colony exhibit up to a tenfold difference in mass, labor is divided by body size. Current adaptive explanations for this important life history feature are unsatisfactory. Within the colony, what is the function of the smaller workers? Here, we report on the differential robustness to starvation of small and large worker bumble bees (Bombus impatiens); when nectar is scarce, small workers remain alive significantly longer than larger workers. The presence of small workers, and size variation in general, might act as insurance against times of nectar shortage. These data may provide a novel, adaptive explanation, independent of division of labor, for size polymorphism within the worker caste.     

Population genomics reveals a candidate gene involved in bumble bee pigmentation

Variation in bumble bee color patterns is well‐documented within and between species. Identifying the genetic mechanisms underlying such variation may be useful in revealing evolutionary forces shaping rapid phenotypic diversification. The widespread North American species Bombus bifarius exhibits regional variation in abdominal color forms, ranging from red‐banded to black‐banded phenotypes and including geographically and phenotypically intermediate forms. Identifying genomic regions linked to this variation has been complicated by strong, near species level, genome‐wide differentiation between red‐ and black‐banded forms. Here, we instead focus on the closely related black‐banded and intermediate forms that both belong to the subspecies B. bifarius nearcticus. We analyze an RNA sequencing (RNAseq) data set and identify a cluster of single nucleotide polymorphisms (SNPs) within one gene, Xanthine dehydrogenase/oxidase‐like, that exhibit highly unusual differentiation compared to the rest of the sequenced genome. Homologs of this gene contribute to pigmentation in other insects, and results thus represent a strong candidate for investigating the genetic basis of pigment variation in B. bifarius and other bumble bee mimicry complexes.     

Seasonality, division of labor, and dynamics of colony-level nutrient storage in the ant Pheidole morrisi

Nutritional provisioning is a critical component of life history strategies, and of particular interest in social insect colonies because of the role that division of labor plays in resource allocation. To explore the mechanisms that underlie colony nutritional strategies, I examined three populations of the ant Pheidole morrisi across a gradient of overwinter food scarcity over two seasons. P. morrisi colonies were found to employ amixed strategy of fat storage with regard to a longer overwinter period: members of both worker castes increase their percent-fat in a graded manner, while the proportion of a specialized subcaste of majors known as “repletes”, also increased within the colony. Geographic variation in other colony traits such as mean colony size, mean worker size, and minor/major caste ratio were also found, although not always in a manner clearly relating to fat storage. These results indicate that colony demography responds to seasonal fluctuations in food availability through behavioral alterations (increased fat stores and recruitment of replete workers) rather than physical alterations (changes in lean body sizes or caste ratio). The findings illustrate the dynamic role division of labor plays in the success of insect colonies confronting environmental variability. Received 9 May 2006; revised 19 July 2006; accepted 24 July 2006.