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Production of bumblebees (Hymenoptera: Apidae) for pollination and research
Abstract
Few bumblebee (Bombus) species have been developed for commercial production or mass rearing but domesticating a variety of species could provide commercial pollinators or conservation techniques for threatened wild populations. While it is apparent that some variety in rearing protocols tailored to species specificity is required, a core methodological foundation is critical across multiple species and rearing programs. The methods presented herein aim to highlight protocols that foster safe and efficient rearing conditions, minimize husbandry requirements, and mitigate pathogen transfer across North America. Promoting broodiness and colony initiation in wild-caught foundress queens, and successfully overwintering gynes for a duration that mimics the natural bumblebee lifecycle remain major challenges to rearing bumblebees, ex situ. Advancements in bumblebee rearing techniques are ongoing, but standardization and transparency of protocols across the rearing community remain of primary importance.
... Bombus vosnesenskii is now one of 2 bumble bee species currently available for commercial production in the United States, where it can be purchased for crop pollination throughout its native range (Koppert 2022). Although, B. vosnesenskii are commercially produced, little information is publicly available regarding rearing methods, nest success, and developmental timelines (Rowe et al. 2023, Strange et al. 2023. Previous research identified that B. vosnesenskii have high nest success in a controlled laboratory setting (Rowe et al. 2023, Strange et al. 2023. ...
... Bombus vosnesenskii is now one of 2 bumble bee species currently available for commercial production in the United States, where it can be purchased for crop pollination throughout its native range (Koppert 2022). Although, B. vosnesenskii are commercially produced, little information is publicly available regarding rearing methods, nest success, and developmental timelines (Rowe et al. 2023, Strange et al. 2023. Previous research identified that B. vosnesenskii have high nest success in a controlled laboratory setting (Rowe et al. 2023, Strange et al. 2023. ...
... Although, B. vosnesenskii are commercially produced, little information is publicly available regarding rearing methods, nest success, and developmental timelines (Rowe et al. 2023, Strange et al. 2023. Previous research identified that B. vosnesenskii have high nest success in a controlled laboratory setting (Rowe et al. 2023, Strange et al. 2023. For example, from 2014 to 2019, 48.2% of wild-caught B. vosnesenskii gynes produced brood (nest initiation), and 25.2% had one worker eclose (nest establishment) (Strange et al. 2023). ...
Bombus vosnesenskii Radowszkowski, 1862 is one of three bumble bee species commercially available for pollination services in North America; however, little is documented about B. vosnesenskii colony life cycle or the establishment of ex situ rearing, mating, and overwintering practices. In this study, we documented nest success, colony size, and gyne production; recorded the duration of mating events; assessed overwintering survival of mated gynes; and evaluated second-generation nest success for colonies established from low- and high-elevation wild-caught B. vosnesenskii gynes. Of the 125 gynes installed, 62.4% produced brood cells (nest initiation) and 43.2% had at least 1 worker eclose (nest establishment). High-elevation B. vosnesenskii gynes had significantly higher nest initiation and establishment success than low-elevation gynes. However, low-elevation colonies were significantly larger with queens producing more gynes on average. Mating was recorded for 200 low-elevation and 37 high-elevation gynes, resulting in a mean duration of 62 and 51 min, respectively. Mated gynes were then placed into cold storage for 54 days to simulate overwintering, which resulted in 59.1% of low-elevation gynes surviving and 91.9% of high-elevation gynes surviving. For second-generation low-elevation gynes, 26.4% initiated nesting and 14.3% established nesting. Second-generation high-elevation gynes did not initiate nesting despite CO2 narcosis treatments. Overall, these results increase our understanding of B. vosnesenskii nesting, mating, and overwintering biology from 2 elevations. Furthermore, this study provides information on successful husbandry practices that can be used by researchers and conservationists to address knowledge gaps and enhance the captive rearing of bumble bees.
... Recent efforts toward rearing bumble bees in captivity have improved techniques available to conservationists and researchers, which can be used to assess the commercial viability of nondomesticated Bombus species and to establish conservation techniques for imperiled species (Macfarlane et al. 1994, Strange et al. 2011, Christman et al. 2022, Rowe et al. 2023. For example, conservation propagation methods (i.e., assisted reintroductions) have been proposed as a recovery action to augment wild populations (Smith et al. 2020). ...
... The captured gynes were transferred from nets to individual 7 × 3 cm plastic vials (W. W. Grainger Inc., Lake Forest, IL) modified to have ventilation holes (Rowe et al. 2023). The gynes were then transported in chilled, insulated containers to the United States Department of Agriculture-Agricultural Research Service, Pollinating Insect-Biology, Management, and Systematics Research Unit in Logan, UT. ...
... The gynes were then transported in chilled, insulated containers to the United States Department of Agriculture-Agricultural Research Service, Pollinating Insect-Biology, Management, and Systematics Research Unit in Logan, UT. Once at the laboratory, colonies were initiated following methodology outlined in Rowe et al. (2023). Briefly, the gynes were moved into 15 cm × 15 cm × 10 cm plastic rearing chambers (Biobest Canada, Leamington, ON, Canada) in a designated rearing space maintained at 28 ± 2 °C and 65 ± 2% relative humidity in complete darkness. ...
Of the 265 known bumble bee (Bombus) species, knowledge of colony lifecycle is derived from relatively few species. As interest in Bombus commercialization and conservation grows, it is becoming increasingly important to understand colony growth dynamics across a variety of species since variation exists in nest success, colony growth, and reproductive output. In this study, we reported successful nest initiation and establishment rates of colonies and generated a timeline of colony development for 15 western North American Bombus species, which were captively reared from wild-caught gynes from 2009 to 2019. Additionally, we assessed variation in colony size among 5 western North American Bombus species from 2015 to 2018. Nest initiation and establishment rates varied greatly among species, ranging from 5-76.1% and 0-54.6%, respectively. Bombus griseocollis had the highest rates of nest success across the 11-yr period, followed by B. occidentalis, B. vosnesenskii, and B. huntii. Furthermore, days to nest initiation and days to nest establishment varied among species, ranging from 8.4 to 27.7 days and 32.7 to 47 days. Colony size also differed significantly among species with B. huntii and B. vosnesenskii producing more worker/drone cells than B. griseocollis, B. occidentalis, and B. vancouverensis. Additionally, gyne production differed significantly among species with B. huntii colonies producing more gynes than B. vosnesenskii. Results from this study increase knowledge of systematic nesting biology for numerous western North American Bombus species under captive rearing conditions, which can further improve rearing techniques available to conservationists and researchers.
... Further, the vast majority of studies of heat stress effects are done in the laboratory using commercially available B. terrestris and B. impatiens (Table 1), so we have little information on most wild bumble bee species (but see Gerard et al., 2022a;Martinet et al., 2015;Martinet et al., 2021b) in wild settings. This may in part reflect the difficulty in starting colonies from wild caught queens (Christman et al., 2022;Rowe et al., 2023), a challenge we'll need to overcome if we are to better understand species-specific responses to ongoing climate change. ...
Global declines in abundance and diversity of insects are now well-documented and increasingly concerning given the critical and diverse roles insects play in all ecosystems. Habitat loss, invasive species, and anthropogenic chemicals are all clearly detrimental to insect populations, but mounting evidence implicates climate change as a key driver of insect declines globally. Warming temperatures combined with increased variability may expose organisms to extreme heat that exceeds tolerance, potentially driving local extirpations. In this context, heat tolerance limits (e.g., critical thermal maximum, CT max ) have been measured for many invertebrates and are often closely linked to climate regions where animals are found. However, temperatures well below CT max may also have pronounced effects on insects, but have been relatively less studied. Additionally, many insects with out-sized ecological and economic footprints are colonial (e.g., ants, social bees, termites) such that effects of heat on individuals may propagate through or be compensated by the colony. For colonial organisms, measuring direct effects on individuals may therefore reveal little about population-level impacts of changing climates. Here, we use bumble bees (genus Bombus ) as a case study to highlight how a limited understanding of heat effects below CT max and of colonial impacts and responses both likely hinder our ability to explain past and predict future climate change impacts. Insights from bumble bees suggest that, for diverse invertebrates, predicting climate change impacts will require a more nuanced understanding of the effects of heat exposure and additional studies of carry-over effects and compensatory responses by colonies.
... A typical honeybee colony is made up of a queen bee, tens of thousands of female workers, and a few thousand male drone bees. The primary role of a queen bee is to lay eggs, while the drone's purpose is to mate with the queen (Rowe et al., 2023). Female bees produce honey, ensure the cleanliness of the hive, protect the hive and honey, and take care of the queen and larvae. ...
Over the past few decades, traditional medicinal products have grown in popularity. It is estimated that 80% of patients worldwide use them for basic health treatment. Due to its extraordinary bioactive properties, propolis is a bee product commonly utilised in alternative medicines. Propolis is a complicated mixture of substances, procured by bees from diverse vegetations and mix them with beeswax and bee saliva enzymes. Propolis bioactivities have been examined and reported in the treatments of numerous chronic diseases. Given the differences in pharmacological activity and compound markup of propolis, huge variation exists due to numerous hive localities. This study intends to define and explore the bioactive qualities of propolis in Malaysia. Information on the antibacterial, antioxidant, anti-inflammatory, and other bioactivity properties from studies conducted on Malaysian propolis have been consolidated in this review. This research would result in an enhanced understanding of the safe consumption of Malaysian propolis and may spur the development of novel and more affordable treatments for various infections.
Pollen is an essential component of bee diets, and rearing bumble bees (Bombus spp.) for commercial use necessitates feeding pollen in mass quantities. This pollen is collected from honey bee (Apis mellifera L.) colonies because neither an artificial diet nor an economical, large-scale pollen collection process from flowers is available. The provenance of honey bee-collected pollen is often unknown, and in some cases has crossed international borders. Both deformed wing virus (DWV) and the fungal pathogen Ascosphaera apis (Claussen) Olive & Spiltoir (cause of chalkbrood disease); occur in honey bee-collected pollen, and infections have been observed in bumble bees. We used these pathogens as general surrogates for viruses and spore-forming fungal diseases to test the efficacy of 3 sterilization methods, and assessed whether treatment altered pollen quality for the bumble bee. Using honey bee-collected pollen spiked with known doses of DWV and A. apis, we compared gamma irradiation (GI), ozone fumigation (OZ), and ethylene oxide fumigation (EO) against an untreated positive control and a negative control. Following sterilization treatments, we tested A. apis spore viability, detected viral presence with PCR, and tested palatability to the bumble bee Bombus impatiens Cresson. We also measured bacterial growth from pollens treated with EO and GI. GI and EO outperformed OZ treatment in pathogen suppression. EO had the highest sterilizing properties under commercial conditions and retained palatability and supported bee development better than other treatments. These results suggest that EO sterilization reduces pathogen risks while retaining pollen quality as a food source for rearing bumble bees.
Recent bumble bee declines have prompted the development of novel population monitoring tools, including the use of putatively non-lethal tarsal clipping to obtain genetic material. However, the potential side effects of tarsal clipping have only been tested in the worker caste of a single domesticated species, prompting the need to more broadly test whether tarsal clipping negatively affects sampled individuals. To determine if tarsal clipping reduces queen survivorship and colony establishment, we collected wild queens of Bombus vosnesenskii and clipped tarsi from a single leg of half the individuals. We reared captive queens and estimated survivorship and nest establishment success. We also clipped tarsi of workers from a subset of colonies across a range of body sizes. We found no consistent negative effect of clipping on queen survival. In the first year, clipped nest-searching queens suffered heavy mortality, but there was no effect on foraging queens. The following year, we found no effect of clipping on queen survival or establishment. Clipping did not reduce overall worker survival but reduced survivorship for those in the smallest size quartile.
Implications for insect conservation
Our findings suggest tarsal clipping does not have consistent negative effects on individual survival. However, our results varied with queen behavioral state, year, and worker size, suggesting differences within and among species and interactions with landscape stressors warrant further study. In the interim, we recommend researchers and conservationists minimize the use of tarsal clipping for sensitive species, populations, or small workers except in cases of exceptional scientific need.
The pollen stores of bumble bees host diverse microbiota that influence overall colony fitness. Yet, the taxonomic identity of these symbiotic microbes is relatively unknown. In this descriptive study, we characterized the microbial community of pollen provisions within captive-bred bumble bee hives obtained from two commercial suppliers located in North America. Findings from 16S rRNA and ITS gene-based analyses revealed that pollen provisions from the captive-bred hives shared several microbial taxa that have been previously detected among wild populations. While diverse microbes across phyla Firmicutes, Proteobacteria, Bacteroidetes, Actinobacteria, and Ascomycota were detected in all commercial hives, significant differences were detected at finer-scale taxonomic resolution based on the supplier source. The causative agent of chalkbrood disease in honey bees, Ascosphaera apis, was detected in all hives obtained from one supplier source, although none of the hives showed symptoms of infection. The shared core microbiota across both commercial supplier sources consisted of two ubiquitous bee-associated groups, Lactobacillus and Wickerhamiella/Starmerella clade yeasts that potentially contribute to the beneficial function of the microbiome of bumble bee pollen provisions.
For social bees, an understudied step in evaluating pesticide risk is how contaminated food entering colonies affects residing offspring development and maturation. For instance, neurotoxic insecticide compounds in food could affect central nervous system development predisposing individuals to become poorer task performers later-in-life. Studying bumblebee colonies provisioned with neonicotinoid spiked nectar substitute, we measured brain volume and learning behaviour of 3 or 12-day old adults that had experienced in-hive exposure during brood and/or early-stage adult development. Micro-computed tomography scanning and segmentation of multiple brain neuropils showed exposure during either of the developmental stages caused reduced mushroom body calycal growth relative to unexposed workers. Associated with this was a lower probability of responding to a sucrose reward and lower learning performance in an olfactory conditioning test. While calycal volume of control workers positively correlated with learning score, this relationship was absent for exposed workers indicating neuropil functional impairment. Comparison of 3- and 12-day adults exposed during brood development showed a similar degree of reduced calycal volume and impaired behaviour highlighting lasting and irrecoverable effects from exposure despite no adult exposure. Our findings help explain how the onset of pesticide exposure to whole colonies can lead to lag-effects on growth and resultant dysfunction.
Pollinator nutritional ecology provides insights into plant–pollinator interactions, coevolution, and the restoration of declining pollinator populations. Bees obtain their protein and lipid nutrient intake from pollen, which is essential for larval growth and development as well as adult health and reproduction. Our previous research revealed that pollen protein to lipid ratios (P:L) shape bumble bee foraging preferences among pollen host-plant species, and these preferred ratios link to bumble bee colony health and fitness. Yet, we are still in the early stages of integrating data on P:L ratios across plant and bee species. Here, using a standard laboratory protocol, we present over 80 plant species’ protein and lipid concentrations and P:L values, and we evaluate the P:L ratios of pollen collected by three bee species. We discuss the general phylogenetic, phenotypic, behavioral, and ecological trends observed in these P:L ratios that may drive plant–pollinator interactions; we also present future research questions to further strengthen the field of pollination nutritional ecology. This dataset provides a foundation for researchers studying the nutritional drivers of plant–pollinator interactions as well as for stakeholders developing planting schemes to best support pollinators.
Bumblebees are important pollinating insects, but many species have suffered declines over the last century. Long-tongued bumblebees have been identified as particularly at risk, partly due to their more selective diet. Attempts to study these species in captivity have been impeded by stress-induced behaviours which cause queens to kill or abandon their brood. Here, we attempt to further develop techniques, using queen pairing and Bombus terrestris cocoons, to successfully rear two common long-tongued bumblebee species (B. pascuorum and B. hortorum) in captivity. Approximately half of queens laid eggs and 29% produced workers. Although challenges remain, there is a great deal to be gained from optimising the captive rearing of these species.
Teeming within pollen provisions are diverse communities of symbiotic microbes, which provide a variety of benefits to bees. Microbes themselves may represent a major dietary resource for developing bee larvae. Despite their apparent importance in sustaining bee health, evidence linking pollen-borne microbes to larval health is currently lacking. We examined the effects of microbe-deficient diets on the fitness of larval mason bees. In a series of diet manipulations, microbe-rich maternally collected pollen provisions were replaced with increasing fractions of sterilized, microbe-deficient pollen provisions before being fed to developing larvae. Convergent findings from amino acid and fatty acid trophic biomarker analyses revealed that larvae derived a substantial amount of nutrition from microbial prey and occupied a significantly higher trophic position than that of strict herbivores. Larvae feeding on increasingly sterile diets experienced significant adverse effects on growth rates, biomass and survivorship. When completely deprived of pollen-borne microbes, larvae consistently exhibited marked decline in fitness. We conclude that microbes associated with aged pollen provisions are central to bee health, not only as nutritional mutualists, but also as a major dietary component. In an era of global bee decline, the conservation of such bee-microbe interactions may represent an important facet of pollinator protection strategies.
Bombus impatiens, the common eastern bumble bee, is the first bumble bee established outside of its native range in North America. Native to the eastern portion of the continent, the species was imported to British Columbia in the early 2000s for greenhouse pollination and subsequently became established in the wild. Here we report on the continuing expansion of its range in the Pacific Northwest, including the detection of gynes and workers in Washington State. Sightings of B. impatiens in the region have become increasingly common based on various Internet mapping and reporting sites. The species has been observed about 30 km south of the British Columbia border, or 60 km from the first British Columbia detections. Species distribution models indicate that the Puget Sound and Willamette Valley are suitable habitat, and the bee will likely continue to expand its range southward towards California. The potential impacts of B. impatiens in the region are unknown and will be monitored in future research.
Foraging behavior is a critical adaptation by insects to obtain appropriate nutrients from the environment for development and fitness. Bumble bees (Bombus spp.) form annual colonies which must rapidly increase their worker populations to support rearing reproductive individuals before the end of the season. Therefore, colony growth and reproduction should be dependent on the quality and quantity of pollen resources in the surrounding landscape. Our previous research found that B. impatiens foraging preferences to different plant species were shaped by pollen protein:lipid nutritional ratios (P:L), with foragers preferring pollen species with a ~5:1 P:L ratio. In this study, we placed B. impatiens colonies in three different habitats (forest, forest edge, and valley) to determine whether pollen nutritional quality collected by the colonies differed between areas that may differ in resource abundance and diversity. We found that habitat did not influence the collected pollen nutritional quality, with colonies in all three habitats collecting pollen averaging a 4:1 P:L ratio. Furthermore, there was no difference in the nutritional quality of the pollen collected by colonies that successfully reared reproductives and those that did not. We found however, that “nutritional intake,” calculated as the colony‐level intake rate of nutrient quantities (protein, lipid, and sugar), was strongly related to colony growth and reproductive output. Therefore, we conclude that B. impatiens colony performance is a function of the abundance of nutritionally appropriate floral resources in the surrounding landscape. Because we did not comprehensively evaluate the nutrition provided by the plant communities in each habitat, it remains to be determined how B. impatiens polylectic foraging strategies helps them select among the available pollen nutritional landscape in a variety of plant communities to obtain a balance of key macronutrients.
Crithidia bombi and Crithidia expoeki (Trypanosomatidae) are common parasites of bumble bees (Bombus spp.). Crithidia bombi was described in the 1980s, and C. expoeki was recently discovered using molecular tools. Both species have cosmopolitan distributions among their bumble bee hosts, but there have been few bumble bee studies that have identified infections to species since the original description of C. expoeki in 2010. Morphological identification of species is difficult due to variability within each stage of their complex lifecycles, although they can be easily differentiated through DNA sequencing. However, DNA sequencing can be expensive, particularly with many samples to diagnose. In order to reliably and inexpensively distinguish Crithidia species for a large-scale survey, we developed a multiplex PCR protocol using species-specific primers with a universal trypanosomatid primer set to detect unexpected relatives. We applied this method to 356 trypanosomatid-positive bumble bees from North America as a first-look at the distribution and host range of each parasite in the region. Crithidia bombi was more common (90.2%) than C. expoeki (21.3%), with most C. expoeki-positive samples existing as co-infections with C. bombi (13.8%). This two-step detection method also revealed that 2.2% samples were positive for trypanosmatids that were neither C. bombi nor C. expoeki. Sequencing revealed that two individuals were positive for C. mellificae, one for Lotmaria passim, and three for two unclassified trypanosomatids. This two-step method is effective in diagnosing known bumble bee infecting Crithidia species, and allowing for the discovery of unknown potential symbionts.
Microsporidium Nosema ceranae is well known for exerting a negative impact on honey bee health, including down-regulation of immunoregulatory genes. Protein nutrition has been proven to have beneficial effects on bee immunity and other aspects of bee health. Bearing this in mind, the aim of our study was to evaluate the potential of a dietary amino acid and vitamin complex “BEEWELL AminoPlus” to protect honey bees from immunosuppression induced by N. ceranae. In a laboratory experiment bees were infected with N. ceranae and treated with supplement on first, third, sixth and ninth day after emergence. The expression of genes for immune-related peptides (abaecin, apidaecin, hymenoptaecin, defensin and vitellogenin) was compared between groups. The results revealed significantly lower (p<0.01 or p<0.001) numbers of Nosema spores in supplemented groups than in the control especially on day 12 post infection. With the exception of abacein, the expression levels of immune-related peptides were significantly suppressed (p<0.01 or p<0.001) in control group on the 12th day post infection, compared to bees that received the supplement. It was supposed that N. ceranae had a negative impact on bee immunity and that the tested amino acid and vitamin complex modified the expression of immune-related genes in honey bees compromised by infection, suggesting immune-stimulation that reflects in the increase in resistance to diseases and reduced bee mortality. The supplement exerted best efficacy when applied simultaneously with Nosema infection, which can help us to assume the most suitable period for its application in the hive.
Bumble bees are highly valued crop pollinators, particularly in greenhouses, but their use carries risks for wild bumble bee populations. Effective techniques to rear bumble bees for use as commercial pollinators were developed during the 20th century. Bumble bee rearing efforts date back to the 1890s, but year-round production of bumble bee colonies was not possible until the late 1980s. The bumble bee rearing industry grew rapidly in the 1990s as the popularity of bumble bee use for greenhouse pollination of tomatoes increased. The commercial production of bumble bees led to a boom in their use, primarily in greenhouses. A small number of species are commercially reared by a small number of companies and transported around the globe. This has raised concerns about potential negative ecological effects including introduction of non-native bumble bee species or subspecies, introduction of non-native genotypes, introduction of traits selected by commercial rearing, introduction of novel or more virulent pests and parasites, and disruption of native plant pollination. Mitigation efforts include increased efforts to monitor commercial stock for pathogens and parasites, preventing escape of bumble bees from greenhouses, creating more effective regulation of managed bumble bee transport, reliance on wild bumble bee populations for field pollination, and rearing of local species or sub-species. The use of commercially raised bumble bee colonies for crop pollination need not come at the risk of the health of wild, native bumble bee populations
Bee population declines are linked to reduction of nutritional resources due to land-use intensification, yet we know little about the specific nutritional needs of many bee species. Pollen provides bees their primary source of protein and lipids, but nutritional quality varies widely among host-plant species. Therefore, bees may be adapted to assess resource quality and adjust their foraging behavior to balance nutrition from multiple food sources. We tested the ability of two bumble bee species, Bombus terrestris and B. impatiens, to regulate protein and lipid intake. We restricted B. terrestris adults to single synthetic diets varying in protein:lipid ratios (P:L). The bees overate protein on low fat diets and overate lipid on high fat diets to reach their targets of lipid and protein respectively. The bees survived best on a 10:1 P:L diet; the risk of dying increased as a function of dietary lipid when bees ate diets with lipid contents greater than 5:1 P:L. Hypothesizing that P:L intake target of adult worker bumble bees was between 25:1-5:1, we presented workers from both species unbalanced but complementary paired diets to determine if they self-select their diet to reach a specific intake target. Bees consumed similar amounts of proteins and lipids in each treatment and averaged a 14:1 P:L for B. terrestris and 12:1 P:L for B. impatiens These results demonstrate that adult worker bumble bees likely select foods that provide them with a specific ratio of P:L. These P:L intake targets could affect pollen foraging in the field and help explain patterns of host-plant species choice by bumble bees.
Significance
Bees pollinate the majority of flowering plant species, including agricultural crops. The pollen they obtain is their main protein and lipid source that fuels development and reproduction. Bee populations are declining globally, in large part because of landscape-level loss of host-plant species contributing to a nutritional shortage. To mitigate declines, we must understand how the nutritional requirements of bees influence foraging behavior. We demonstrate that bumble bees selectively collect pollen from host-plant species based on the protein:lipid ratios of pollen. Our research indicates that bees evaluate pollen quality and adjust foraging decisions to meet their nutritional needs. To be effective, conservation initiatives must include host-plant species that provide pollen that satisfies the nutritional demands of bees to support their populations.
Those involved with pollinator risk assessment know that agricultural crops vary in attractiveness to bees. Intuitively this means that exposure to agricultural pesticides is likely greatest for attractive plants and lowest for unattractive plants. While crop attractiveness in the risk assessment process has been qualitatively remarked on by some authorities, absent is direction on how to refine the process with quantitative metrics of attractiveness. At a high level, attractiveness of crops to bees appears to depend on several key variables, including but not limited to: floral, olfactory, visual and tactile cues, seasonal availability, physical and behavioral characteristics of the bee and plant, and nectar rewards. Notwithstanding the complexities and interactions amongst these variables, sugar content in nectar stands out as a suitable quantitative metric by which to refine pollinator risk assessments for attractiveness. Provided herein is a proposed way to use sugar nectar concentration to adjust the exposure parameter (with what is called a Crop Attractiveness Factor) in the calculation of risk quotients in order to derive crop-specific Tier I assessments. This Perspective is meant to invite discussion on incorporating such changes in the risk assessment process.
The mating behaviour of Bombus terresfris was studied using wooden observation cages (50 x 50 x 7O cm) in the laboratory. Queens and males from reared colonies were isolated from the odour of the opposite sex before the experiments. Mating pairs (one per box) consisted of one 1O-day-old virgin male and one 5-day-old virgin queen. The behaviour of each of the 80 pairs used was observed for 15 min, during which time 47 of the pairs copulated. Male behaviour could be divided into approach, inspection and attempt to copulate. Queen reactions to the male were immobility (1 3 .9Vo), threat (53 .9yo) or flight (32.3o/o). Queens could also display inspection behaviour. The mating success of a behavioural sequence was positively correlated with the frequency of inspections by both sexes and negatively correlated with queen immobility. Flow diagrams showing seguences of types of behaviour are presented. The role of sexual pheromones in mating is discussed.
Bees have been managed and utilised for honey production for centuries and, more recently, pollination services. Since the mid 20th Century, the use and production of managed bees has intensified with hundreds of thousands of hives being moved across countries and around the globe on an annual basis. However, the introduction of unnaturally high densities of bees to areas could have adverse effects. Importation and deployment of managed honey bee and bumblebees may be responsible for parasite introductions or a change in the dynamics of native parasites that ultimately increases disease prevalence in wild bees. Here we review the domestication and deployment of managed bees and explain the evidence for the role of managed bees in causing adverse effects on the health of wild bees. Correlations with the use of managed bees and decreases in wild bee health from territories across the globe are discussed along with suggestions to mitigate further health reductions in wild bees.
The rearing method under controlled conditions known for Bombus terrestris was successful in initiating egg-laying for 83% of B. pascuorum queens. After larvae had hatched, fresh pollen pellets needed to be inserted into brood pockets daily. After the first workers had emerged, colony development was advanced by placing them outdoors and supplying them with a sugar solution and pollen. The bees were able to use tightly pressed pollen from small plastic pots inserted near the brood. This feeding resulted in large colonies that produced dozens of young queens. In contrast, colonies managed in the laboratory were unable to utilize pollen in a similar manner. They raised only a few workers and several queens. Mating young queens was easy. It was stimulated by daylight, but in the case of B. humilis by direct sunshine. Several B. pascuorum and B. sylvarum queens were overwintered and began the new generation under artificial conditions. However, a lack of fresh pollen limited the development of colonies outside of the vegetation period.
The dispersal of parasites is critical for epidemiology, and the interspecific vectoring of parasites when species share resources may play an underappreciated role in parasite dispersal. One of the best examples of such a situation is the shared use of flowers by pollinators, but the importance of flowers and interspecific vectoring in the dispersal of pollinator parasites is poorly understood and frequently overlooked. Here, we use an experimental approach to show that during even short foraging periods of 3 h, three bumblebee parasites and two honeybee parasites were dispersed effectively onto flowers by their hosts, and then vectored readily between flowers by non-host pollinator species. The results suggest that flowers are likely to be hotspots for the transmission of pollinator parasites and that considering potential vector, as well as host, species will be of general importance for understanding the distribution and transmission of parasites in the environment and between pollinators.
© 2015 The Author(s).
Bumblebees are important pollinating insects for a wide variety of crops and wild
flowering plants, but many species are experiencing declines throughout the world
due to multiple factors including nutritional stress. Bee nutrition may initially appear
simple, with all species feeding exclusively on pollen and nectar. However, these flower
resources come from a taxonomically diverse range of plants that are varied in their
biochemistry and therefore in the nutritional value of their nectar and pollen. In addition, bumblebee nutritional requirements differ between castes and life-stages,
and there are also a wide variety of differences between bumblebee species in their
life-history traits, including methods of larval feeding and the flower taxa they prefer
to forage on. As with all organisms, suboptimum nutrition (nutritional stress) can have
significant effects on growth, development and survival, but our understanding of nutritional biology in bumblebees comes predominantly from just two species that are not
representative of bumblebees in general, or of the species that are of greatest conservation concern. For the conservation of declining bumblebees and the sustainable
management of healthy commercial colonies, understanding the nutritional biology
of a greater diversity of species should therefore be a priority
Insects maximize their fitness by exhibiting predictable and adaptive seasonal patterns in response to changing environmental conditions. These seasonal patterns are often expressed even when insects are kept in captivity, suggesting they are functionally and evolutionary important.
In this study we examined whether workers of the eusocial bumble bee Bombus impatiens maintained a seasonal signature when kept in captivity. We used an integrative approach and compared worker egg-laying, ovarian activation, body size and mass, lipid content in the fat body, cold tolerance and expression of genes related to cold tolerance, metabolism, and stress throughout colony development.
We found that bumble bee worker physiology and gene expression patterns shift from reproductive-like to diapause-like as the colony ages. Workers eclosing early in the colony cycle had increased egg-laying and ovarian activation, and reduced cold tolerance, body size, mass, and lipid content in the fat body, in line with a reproductive-like profile, while late-eclosing workers exhibited the opposite characteristics. Furthermore, expression patterns of genes associated with reproduction and diapause differed between early- and late-eclosing workers, partially following the physiological patterns.
We suggest that a seasonal signature, innate to individual workers, the queen or the colony is used by workers as a social cue determining the phenology of the colony and discuss possible implications for understanding reproductive division of labor in bumble bee colonies and the evolutionary divergence of female castes in the genus Bombus.
1. Behavior and organization of social groups is thought to be vital to the functioning of societies, yet the contributions of various roles within social groups have been difficult to quantify. A common approach to quantifying these role-based contributions is evaluating the performance of individuals at conducting certain roles, these studies ignore how these performances might scale up to effects at the population-level. Manipulative experiments are another common approach to determine population-level effects, but they often ignore potential feedbacks associated with these various roles.
2. Here, we evaluate the effects of worker size distribution in bumblebee colonies on worker production, using functional linear models. Functional linear models are a recent correlative technique that has been used to assess lag effects of environmental drivers on plant performance. We demonstrate potential applications of this technique to explore contributions of social animals to ecological phenomenon.
3. We found that the worker size distribution differentially affected new worker production across three resource environments. Specifically, more larger workers had mostly positive effects and more smaller workers had negative effects on worker production. Most of these effects were only detected under low or fluctuating resource environments suggesting that the advantage of colonies with larger-bodied workers becomes more apparent under stressful conditions.
4. We demonstrate the wider ecological application of functional linear models. We highlight the advantages and limitations when considering these models, and how they are a valuable complement to many of these performance-based and manipulative experiments.
Parasites are linked to the decline of some bee populations; thus, understanding defense mechanisms has important implications for bee health. Recent advances have improved our understanding of factors mediating bee health ranging from molecular to landscape scales, but often as disparate literatures. Here, we bring together these fields and summarize our current understanding of bee defense mechanisms including immunity, immunization, and transgenerational immune priming in social and solitary species. Additionally, the characterization of microbial diversity and function in some bee taxa has shed light on the importance of microbes for bee health, but we lack information that links microbial communities to parasite infection in most bee species. Studies are beginning to identify how bee defense mechanisms are affected by stressors such as poor-quality diets and pesticides, but further research on this topic is needed. We discuss how integrating research on host traits, microbial partners, and nutrition, as well as improving our knowledge base on wild and semi-social bees, will help inform future research, conservation efforts, and management.
Bumble bees (Bombus [Hymenoptera: Apidae]) are important pollinators for agricultural crops, which has led to their commercial domestication. Despite their importance, little is known about the reproductive biology of bumble bees native to North America. The Hunt bumble bee (Bombus huntii Greene [Hymenoptera: Apidae]) and the Vosnesensky bumble bee (Bombus vosnesenskii Radoszkowski [Hymenoptera: Apidae] are native candidates for commercial production in western North America due to their efficacy in providing commercial pollination services. Availability of pollinators native to the region in which services would be provided would minimize the likelihood of introducing exotic species and spreading novel disease. Some parasites are known to affect bumble bee reproduction, but little is known about their prevalence in North America or how they affect queen success. Only 38% of wild-caught B. huntii and 51% wild-caught B. vosnesenskii queens collected between 2015 and 2017 initiated nests in the laboratory. Our objective was to identify causal factors leading to a queen's inability to oviposit. To address this, we dissected each broodless queen and diagnosed diseases, assessed mating status, and characterized ovary development. Nematodes, arthropods, and microorganisms were detected in both species. Overall, 20% of queens were infected by parasites, with higher rates in B. vosnesenskii. Over 95% of both species were mated, and over 88% had developed ovaries. This suggests that parasitism and mating status were not primary causes of broodlessness. Although some failure to nest can be attributed to assessed factors, additional research is needed to fully understand the challenges presented by captive rearing.
Bumble bees provide valuable pollination services to many wild and agricultural plants. Populations of some bumble bee species are in decline, prompting the need to better understand bumble bee biology and to develop methodologies for assessing the effects of environmental stressors on these bees. Use of bumble bee microcolonies as an experimental tool is steadily increasing. This review closely examines the microcolony model using peer-reviewed published literature identified by searching three databases through November 2018. Microcolonies have been successfully used for investigating a range of endpoints including behavior, the gut microbiome, nutrition, development, pathogens, chemical biology, and pesticides/xenobiotics. Methods for the initiation and monitoring of microcolonies, as well as the recorded variables were catalogued and described. From this information, we identified a series of recommendations for standardizing core elements of microcolony studies. Standardization is critical to establishing the foundation needed to support use of this model for biological response investigations and particularly for supporting use in pesticide risk assessment.
Many insects sequester nutrients during developmentally programmed periods, which they metabolize during subsequent life history stages. During these periods, failure to store adequate nutrients can have persistent effects on fitness. Here, we examined a critical but under-studied nutrient storage period in queen bumble bees: the first days of adult life, which are followed by a diapause period typically coinciding with winter. We experimentally manipulated availability of pollen (the primary dietary source of lipids and protein) and the sugar concentration of artificial nectar (the primary source of carbohydrates) for laboratory-reared queens during this period and examined three nutritional phenomena: (i) diet impacts on nutritional status, (ii) the timescale upon which nutrient sequestration occurs and (iii) the fitness consequences of nutrient sequestration, specifically related to survival across the life cycle. We found evidence that pollen and nectar starvation negatively impact lipid storage, whereas nectar sugar concentration impacts stored carbohydrates. The majority of nutrients were stored during the first ~ 3 days of adult life. Nutrients derived from pollen during this period appear to be more critical for surviving earlier life stages, whereas nutrients sequestered from nectar become more important for surviving the diapause and post-diapause periods. Negative impacts of a poor diet during early life persisted in our experiment, even when pollen and a relatively high (50%) nectar sugar concentration were provided post-diapause. Based on these findings, we posit that the nutritional environment during the early adult life of queens has both immediate and persistent impacts on fitness. These findings underscore the importance of examining effects of stage-specific nutritional limitations on physiology and life history traits in this social insect group. Moreover, the findings may shed light on how declining food resources are contributing to the decline of wild bumble bee populations.
Bumble bees are generalist pollinators that typically collect floral rewards from a wide array of flowering plant species. Among the greatest threats to wild bumble bee populations worldwide, many of which are declining, is a loss of floral resource abundance and diversity in the landscapes they inhabit. We examined how composition of pollen diet impacts early nesting success in laboratory-reared queens of the bumble bee Bombus impatiens. Specifically, we provided queens and their young nests with one of three pollen diets, each of which was dominated by a single pollen type, and explored how this diet treatment influenced the length of time until queens initiated nests, total counts of brood in the nest at the end of the experiment (8 wk later), and the size and weight of adult offspring produced. We found that the amount of later-stage brood (pupae and/or adults) produced by recently-initiated nests was strongly impacted by pollen diet. For example, on average 66% fewer later-stage brood were found in nests provided with the Cistus pollen Linnaeus (Cistaceae), relative to the predominantly Asteraceae pollen. This finding suggests that particular pollen diet compositions may delay larval growth, which delays colony development and may ultimately be detrimental for young nests. This study sheds light on how one of the leading stressors for bumble bees (nutritional stress) may negatively impact populations through its influence on brood production during the nest-founding stage of the colony cycle.
Bumble bees are eusocial, yet queens are solitary for much of their lives. Little is known about the stages in the solitary phase of queens, including the factors that influence successful initiation of nests. One anecdotal recommendation suggests that wild-caught queens are less likely to initiate nests if they are captured while carrying pollen loads. Queens that are collecting pollen have already chosen a nest site and are either preparing to lay their first clutch of eggs, have already begun oviposition, or are provisioning developing brood. Although there is a conservation-based argument for leaving these queens to their own devices, we were interested in the biological aspect of this: if a queen has already initiated a nest in the wild, will she initiate another one in captivity? In 2016 and 2017, 960 queens of five species were captured, and the presence or absence of corbicular loads of pollen was noted. Each queen was then placed in an artificial nest and provided with unlimited food for 21 days. Nests were monitored for brood presence daily, and rates of nest initiation (brood production) were compared between queens captured with and without pollen loads. Nest initiation rates varied among species, as did the influence of pollen-collecting behavior at the time of capture. Pollen-laden Bombus occidentalis queens were less likely to lay eggs, yet B. bifarius and B. vosnesenskii queens with pollen had a greater chance of initiating a captive nest. These results should inform both commercial and conservation efforts.
Exposure to carbon dioxide (CO2) has pleiotropic effects in many insect species, ranging from eliciting rapid behavioral responses such as attraction, to dramatic physiological changes, including ovary activation. In bumble bees, CO2 narcosis causes queens to bypass diapause and initiate egg laying, but its mode of action is not well-understood. Here, we evaluated the effects of CO2 narcosis on the behavior, physiology and immune function of virgin bumble bee queens (Bombus impatiens). We tested the hypothesis that CO2 induces these changes by stimulating oxidative stress response pathways. We found that CO2 stimulates ovarian activation and egg production and suppresses lipid (but not glycogen) accumulation in virgin queens. Additionally, CO2 treated queens were more active (particularly in terms of flight) and performed, but did not receive, more aggressive behaviors compared to controls. Moreover, CO2 positively affected immune function in queens, reduced transcript levels of 5/6 antioxidant enzyme genes and had no effect on longevity. Thus, although CO2 treatment stimulated reproduction, we did not observe any evidence of a trade-off in queen health parameters, aside from a reduction in lipids. Overall CO2 narcosis does not appear to stimulate a typical stress response in virgin bumble bee queens. On the contrary, CO2 narcosis appears to stimulate changes that prepare queens to cope with the nutritional, metabolic and behavioral challenges associated with reproduction and colony-founding.
An investigation of the occurrence and behaviour of honeybees and bumble bees in field beans in 1969 and 1970 showed that the number and percentage of bees entering the mouths of the flowers (positive visits) was greatest in the afternoons. Early in the flowering period the majority of honeybees collected pollen, whereas later in the season they chiefly collected nectar from the extrafloral nectaries or from holes bitten in the calyx and corolla tube by B. terrestris (negative visits). Bumble bees worked more rapidly than honeybees when making positive flower visits, but were considerably less numerous than honeybees. The pollination value of different types of bee visit is discussed.
Significance
Wild bumble bees are experiencing population declines globally. Causes of declines in North American populations are unclear, although declining species are more frequently infected by the pathogen Nosema bombi . A widely accepted hypothesis suggests that contact with European species during domestication led to the introduction of exotic N. bombi . By screening museum specimens, we show that N. bombi prevalence increased significantly in declining species in the early to mid-1990s, coincident with N. bombi outbreaks in North American commercial stocks. There is no evidence that exotic Nosema strains were introduced from Europe. Regardless of geographic origins, the temporal connection between N. bombi epizootics in commercial Bombus stocks and increases in wild populations suggests a substantial risk of pathogen transmission with domestication.
Bumble bee (Bombus) species are ecologically and economically important pollinators, and many species are in decline. In this article, we develop a mechanistic model to analyse growth trajectories of Bombus vosnesenskii colonies in relation to floral resources and land use. Queen production increased with floral resources and was higher in semi-natural areas than on conventional farms. However, the most important parameter for queen production was the colony growth rate per flower, as opposed to the average number of available flowers. This result indicates the importance of understanding mechanisms of colony growth, in order to predict queen production and enhance bumble bee population viability. Our work highlights the importance of interpreting bumble bee conservation efforts in the context of overall population dynamics and provides a framework for doing so.
Bombus terrestris queens which had been overwintered in artificial conditions were transferred to small wooden boxes in a climate room at 28°C and 65% RH; the bees were supplied with food and subjected to one of four photoperiodic regimes (L24: DO; L8: D16; L16: D8; LO: D24. The photoperiodic regimes were applied until the queens had produced 10–15 workers, after which colonies were transferred from the small initiation boxes to larger ones to allow nests to increase in colony size. The proportion of queens in each treatment which founded colonies ranged from 42% to 61 %, but no significant difference was detected between photoperiodic regimes. Delays to oviposition were significantly shorter in the L8: D16 regime compared with constant dark and constant light: 33.4 ± 4.9 days, 47.3 ± 4.8 days and 58.9 ± 6.7 days respectively. In the L16: D8 regime the delay (42.4 ± 5.6 days) was not significantly different from that in the L8: D16 regime. The period from the start of brooding attitude to oviposition was significantly reduced by the L8: D16 regime (5.4 ± 0.9 days) compared to constant light, constant dark or L16: D8 (9.0 ± 1.0, 10.1 ± 1.4, and 10.2 ± 1.4 days respectively). In the L8: D16 and L16: D8 regimes the proportion of queens that did not produce progeny queens was significantly higher if oviposition was retarded.
Colonies with 10–42 workers were subjected to ambient temperatures () of 3–38 C. Brood temperature (), the rate of oxygen consumption, the proportion of workers engaged in thermoregulatory behaviors (brood incubation and wing fanning), and the proportion of workers engaged in general brood maintenance were monitored. At was usually maintained at 28–32 C, and the percentage occurrence (incidence) of brood incubation varied inversely with . At , wing fanning associated with a rise in and metabolism was prevalent. The incidence of brood maintenance was highest (40%–80%) at = 25–32 C, when the combined incidence of brood incubation and wing fanning was relatively low. In contrast, the incidence of brood maintenance was <30% at near-freezing and was 0%–10% at . These data suggest that the colonies attempt to regulate at a set-point temperature between 28 and 32 C and that the increased employment of workers for thermoregulation occurred at the expense of brood maintenance.
Mating behaviour of Bombus terrestris, its sperm production and sperm transfer to queens were studied in parallel, under controlled conditions. The mean value of the age of mating was 6.1 days (s.e. = 0.4 days) for queens and 12.1 days (s.e. = 1.3 days) for males. The average sperm content of vasa deferentia ranged between 4000 and 230 000 spermatozoa per male. It increased from emergence up to the sixth day. The age at which males mated extended from the sixth day to day 27. Chances to cause queens to mate dropped dramatically after day 11. Spermatheca contents varied from 5800 to 36 200 spermatozoa after a single copulation with virgin males. The efficiency of mating in terms of sperm transfer to spermatheca was not affected by the age but was reduced by previous copulations of the male.
Commercial rearing of Bumblebees started less than 10 years ago in the Netherlands and in Belgium when it became apparent that Bumblebee pollination could replace hand pollination of greenhouse tomatoes. Since that time Bumblebees pollination of greenhouse tomatoes occurs throughout the world. It appears that catching queens in spring nor the release of many colonies in tomato greenhouses have had a significant effect on the abundance of Bumblebees in nature. In Europe Bombus terrestris L. is the main species used for commercial pollination. Local species are used both in the US and Canada. Importing animal species or subspecies that are new to an area is very risky. Undesired characteristics, diseases or parasites may be imported as well. The risk is especially high if so little is known about the taxonomy, diseases and parasites as was the case with Bumblebees. In the area of distribution of Bombus terrestris mixing of subspecies has taken place and we are heading for a similar situation as is already the case in honeybees. A positive effect of the sudden economic importance of Bumblebees is that it has given an impulse to Bumblebee research. The availability of Bumblebee colonies year-round has made them to popular study objects. Several papers have been published on Bumblebee behavior and on pollination experiments with different crops. Progress has been made with respect to diseases, parasites and commensals. Toxicity tests have been developed and Bumblebees are now added to the list of beneficial insects that can be tested for undesireable side effects of pesticides.
The hibernated queens of seven Korean native bumblebee species were collected throughout Korea from March 23 to May 14, 1999. Among them, three species, B. ignitus, B. ardens ardens and B. hypocrita sapporoensis, established colonies under laboratory conditions (28~ 29? , 65%; 8L/16D); 48.9%, 38.9% and 25.0%, respectively. The queens of B. ardens ardens and B. hypocrita sapporoensis laid the first brood in five days and B. ignitus in nine days after field collection. The first worker bees of B. ardens ardens, B. ignitus and B. hypocrita sapporoensis emerged in 26 days or 28 days after field collection, respectively. The emergence of the first male of three species, B. ardens ardens, B. hypocrita sapporoensis and B. ignitus took place in 50 days, 64 days and 73 days, with the emergence of new queens in 15, 10 and 7 day intervals. It is also noticeable that a colony of B. ignitus developed to 456 heads with 262 worker bees, 74 males and 120 virgin queens.
Honey has been considered a relatively safe foodstuff due to its compositional properties, with infant botulism caused by Clostridium botulinum being the most prominent health risk associated with it. Our review is focused on the honey microflora along the food chain and evaluates the pathogenic potential of those microorganisms found in honey. This product may contain a great variety of bacteria and, particularly, fungi that eventually entered the food chain at an early stage (e.g. via pollen). For many of these microorganisms, opportunistic infections in humans have been recorded (e.g. infections by Staphylococcus spp., Citrobacter spp., E. coli, Hafnia alvei, Aspergillus spp., Fusarium spp., Trichoderma spp., Chaetomium spp.), although direct infections via honey were not registered.
The crystalline structure of foods is important to product quality, texture, and stability. It is this crystalline structure and other structural elements that determine product appearance, mechanical properties during handling, mouthfeel during consumption, and shelf stability. To control crystallization, it is necessary to have an understanding of the phase behavior of the system, some knowledge of nucleation and growth kinetics, and the effects of both formulation and processing conditions on this kinetics. In foods, two circumstances for controlling the formation of crystals can be distinguished: those where the crystals provide an element of structure in the product and those where crystallization is a separation process. There are many factors that influence crystallization in food products. In many products, the goal of crystallization is to generate a certain texture or appearance that makes the product acceptable. Thus, nucleating many crystals that remain small within the product itself is often the goal. There must be many crystals with small mean size and narrow distribution. The crystals also must have the proper shape and/or polymorph to enhance stability of the product during storage and distribution. However, in other types of products, crystallization is undesired even though the system is supersaturated. In these cases, techniques are used to prevent crystallization from occurring during storage, because this leads to unacceptable product quality.
This study investigated the effect of the photoperiodic regimes 0 h light : 24 h dark (LD 0:24), LD 8:16, LD 16:8 and LD 24:0 at 28 degrees C and 50% Relative Humidity (RH) on the colony development of hibernated (2.0, 2.5, 3.0, 3.5 and 4.0 months) bumblebee queens. The queens which had hibernated for 3.0 months and which were reared in a LD 8:16 photoperiod showed the highest rate of colony initiation (88.2%), colony foundation (67.6%) and progeny queen production (38.2%). The photoperiod LD 8:16 also produced the shortest period of colony initiation and colony foundation. The highest number of sexual males (171.2 +/- 12.2) and queens (91.2 +/- 9.9) were produced in the colonies when 3.5 and 3.0 month hibernated queens were kept in an LD 8:16 photoperiod. The results show that light regime and hibernation duration affect colony characteristics of Bombus terrestris.
