Male Bumblebees Research Articles

Elevated developmental temperature affects gene expression and oxidative stress in bumblebee (Bombus terrestris) workers

Climate change can negatively impact bumblebee populations, which are crucial pollinators in agricultural systems and natural ecosystems. Bumblebee nest temperatures typically range from 27 to 32 °C, and workers engage in wing fanning to maintain a nest temperature below 32 °C. We investigated the gene expression profile in queen, worker, and male bumblebees (Bombus terrestris) at 27 °C, which is the optimal ambient temperature, and 32 °C, which is the upper-temperature limit requiring wing fanning. We found that a developmental temperature of 32 °C significantly increased the expression of genes related to growth, immune response, antioxidants, and chaperones in workers. Compared to workers reared at 27 °C, those reared at 32 °C exhibited a significant increase in reactive oxygen species (ROS) and iron concentrations in the hemolymph. Additionally, the gene expression of superoxide dismutase (SOD) and transferrin (Tf) was significantly increased in workers at 32 °C. These findings indicate that a developmental temperature of 32 °C in bumblebees, especially workers, leads to an increase in gene expression, including SOD and TF, in response to thermal stress.

Male-biased night foraging by bumblebees (Hymenoptera, Apidae, Bombus spp.) in Taiwan

Known nocturnal behaviors of bees in the superfamily Apoidea, including the genus Bombus, were almost exclusively of females. Here we report observations of active free-ranging male Bombus at night in the plant nursery of the Fushan Research Center, Taiwan, in April 2022. Nectar feeding by males at inflorescences was confirmed by tongue-licking in the absence of pollen collecting. The numbers of active female and male bumblebees during the daytime were close to equal. In contrast, only males were found to be active in the night. Our observations suggest that such nocturnal activity is facultative. This finding not only provides a rare case of nocturnal activity in free-ranging Bombus, but also demonstrates that such behaviors can vary between the sexes.

Effects of Polyploidization on Locomotor and Flight Activity, and Body Size of Males in Japanese Bumblebee, Bombus ignitus

Polyploid animals are seen in the wild in only a few groups such as planaria, weevils, ants, wasps, and bees. The sex of bumblebees is determined by the single-locus complementary sex determination (sl-CSD) system resulting in females emerging from fertilized eggs and males (normal males, haploid) emerging from unfertilized eggs. However, diploid males (polyploids) emerged from fertilized eggs when the sex-determining locus become homozygous caused by inbreeding due to population contraction. To examine the effects of polyploidization on behavioral characteristics in bumblebee males, Bombus ignitus, haploid and diploid males were compared in locomotor activity, ease of staying inside the hive, and flight activity in a laboratory experiment. The results showed that diploid males had higher locomotor activity levels, were less likely to stay inside the hive, and had lower flight activity levels than haploid males. The reduced flight activity levels may lead to lower mating rates in the field. Furthermore, the body size of diploid males was smaller than that of haploid males. Diploid males of bumblebees have a low reproductive and produce diploid sperms to emerge sterile triploids, thus creating a considerable genetic load on the population. The behavioral and morphological characteristics of diploid males may unintentionally serve as a mechanism to prevent the emergence of sterile triploids.

Sperm can’t take the heat: Short-term temperature exposures compromise fertility of male bumble bees (Bombus impatiens)

Bumble bee (genus Bombus) populations are increasingly under threat from habitat fragmentation, pesticides, pathogens, and climate change. Climate change is likely a prime driver of bumble bee declines but the mechanisms by which changing climates alter local abundance, leading to shifts in geographic range are unclear. Heat tolerance is quite high in worker bumble bees (CTmax ∼ 48–55 °C), making it unlikely for them to experience these high temperatures, even with climate warming. However, the thermal tolerance of whole organisms often exceeds that of their gametes; many insects can be sterilized by exposure to temperatures well below their upper thermal tolerance. Male bumble bees are independent from the colony and may encounter more frequent temperature extremes, but whether these exposures compromise spermatozoa is still unclear. Using commercially-reared Bombus impatiens colonies, males were reared in the lab and spermatozoa were exposed (in vivo and isolated in vitro) to sublethal temperatures near lower and upper thermal tolerance (CTmin and CTmax, respectively). Heat exposure (45 °C for up to 85 min) reduced spermatozoa viability both for whole males (in vivo; control = 79.5 %, heat exposed = 58 %, heat stupor = 57.7 %) and isolated seminal vesicles (in vitro; control = 85.5 %, heat exposed = 62.9 %). Whole males exposed to 4 °C for 85 min (in vivo; control = 79.2 %, cold = 72.4 %), isolated seminal vesicles exposed to 4 °C for 85 min (in vitro; control = 85.5 %, cold = 85.1 %), and whole males exposed to for 4 °C for 48 h (in vivo; control = 88.7 %, cold = 84.3 %) did not differ significantly in spermatozoa viability. After<85 min at 45 °C, males had significantly reduced spermatozoa viability, suggesting that short-term heat waves below CTmax could strongly reduce the fertility of male bumble bees with potential population-level impacts.

Behavioral roles of biogenic amines in bumble bee males

To compare the behavioral roles of biogenic amines in the males of primitive and advanced eusocial bees, we determined the levels of dopamine- and octopamine-related substances in the brain, and the behavioral effects of these monoamines by drug injection in the primitive eusocial bumble bee, Bombus ignitus. The levels of dopamine and its precursors in the brain peaked at the late pupal stage, but the dopamine peak extended to adult emergence. The tyramine and octopamine levels increased from the mid-pupal to adult stages. The locomotor and flight activities, and light preference increased with age. Injection of octopamine and its receptor antagonist had significant effects on the locomotor and flight activities, whereas dopamine injection did not, indicating that these activities can be regulated by the octopaminergic system. We also determined the dynamics of dopamine-related substances in honey bee (Apis mellifera) drones. The changes in the dopamine level in the brains of honey bee drones exhibited two peaks from the pupal to adult stages, whereas the bumble bee males had only one peak. These are consistent with the behavioral functions of dopamine in honey bee drones and ineffectiveness of dopamine injection at the adult stage in bumble bee males.

Hyperabundant black-tailed deer impact endangered Garry oak ecosystem floral and bumblebee communities

Garry oak ( Quercus garryana ) and associated ecosystems (GOAE) are culturally and ecologically significant landscapes home to over 100 Species at Risk. With less than 5% of their original extent remaining in Canada, GOAE require urgent attention to guide management of remnant habitats and protect them from ongoing cumulative threats. The loss of top predators has played a large role in a trophic cascade where hyperabundant black-tailed deer ( Odocoileus hemionus columbianus ) are reshaping plant and animal communities, even within protected areas. The impacts of deer browsing on plant communities is well-documented; however, the impact on pollinators that are essential for the restoration and conservation of GOAEs is still unknown. We tested the hypothesis that deer browsing has an indirect impact on bumblebee populations through their direct negative impact on floral communities. We surveyed deer density, floral communities, and bumblebee abundances across ten islands with differing levels of deer presence in the Salish Sea. We found that deer had a negative effect on the abundance of flowering plants, with an even greater effect on native species that bumblebees rely on for foraging. Deer presence had an indirect negative impact on female bumblebee abundances through the depletion of floral resources. Deer also had a negative impact on male bumblebee abundances, potentially caused by lowered colony success over the season on islands with less floral resources. These findings highlight the importance of immediate deer management to prevent the loss of native pollinators and further, potentially irreversible, ecological degradation of GOAEs.

Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees

Cuckoo bumblebees are a monophyletic group within the genus Bombus and social parasites of free-living bumblebees, upon which they rely to rear their offspring. Cuckoo bumblebees lack the worker caste and visit flowers primarily for their own sustenance and do not collect pollen. Although different flower-visiting behaviours can be expected between cuckoo and free-living bumblebees due to different biological constraints, no study has yet quantified such differences. Here, we provide the first empirical evidence of different flower-visiting behaviours between cuckoo and free-living bumblebees. We recorded the flower-visiting behaviour of 350 individual bumblebees over two years in a wild population of the entomophilous plant Gentiana lutea, of which they are among the main pollinators. In cuckoo bumblebees (28.9% of the total), we only found males, while we found both workers and males in free-living bumblebees. Cuckoo bumblebees visited significantly more flowers for longer time periods than both free-living bumblebee workers and males within whorls, while differences at the whole-plant level were less marked. Free-living bumblebee males visited more flowers and performed slightly longer flower visits than workers. Behavioural differences between cuckoo male bumblebees and free-living bumblebee workers are likely related to different foraging needs, while differences between cuckoo and free-living bumblebee males may be caused by differences in colony development and a delayed mating period of free-living bumblebees. The longer visits made by cuckoo male bumblebees will likely negatively affect plant reproductive success through increased within-plant pollen flow.

How to get rid of diploid bumblebee males – variability in wing size and shape does not allow within‐colony ploidy discrimination

AbstractThe bumblebee Bombus terrestris L. (Hymenoptera: Apidae) is an effective pollinator of both wild and cultivated plants and essential for the pollination of various important greenhouse crops. Because of its sex determination mechanism, homozygosity of the complementary sex determination (csd) locus due to inbreeding causes fertilized eggs to develop into diploid males, which represent a serious disadvantage for the colonies as their presence decreases colony growth and survival. The identification of diploid males is thus important from both ecological and economic points of view. In the present study, we applied the geometric morphometrics method on wing shape and size of B. terrestris diploid and haploid males at overall and intra‐colony levels to investigate wing changes between the two groups. We found that changes in wing shape concerned almost all cells investigated and male diploidy resulted in a narrower and slightly longer configuration. In addition, diploid male wings presented a very high variation both in size and shape, likely due to sub‐optimal temperature of incubation and food availability during their larval development. This strong variation of diploid male wings makes the ploidy discrimination by wing geometric morphometrics inaccurate based on small reference samples at the intra‐colony level even with allometric data correction, whereas it is accurate (precision &gt;90%) at the overall level, in which sample size is high enough (i.e., 500 individuals). Therefore, our results indicated the need to create a large dataset to allow the analysis of few samples, as is the case with studies of wild bumblebee populations, small rearing companies, or preserved museum specimens. For this reason, we provide a large database of B. terrestris wing Procrustes coordinates (500 samples) to the bumblebee scientific community for use in the analysis of the determination of diploid male individuals.

Thiamethoxam as an inadvertent anti-aphrodisiac in male bees

Sexual reproduction is common to almost all multi-cellular organisms and can be compromised by environmental pollution, thereby affecting entire populations. Even though there is consensus that neonicotinoid insecticides can impact non-target animal fertility, their possible impact on male mating success is currently unknown in bees. Here, we show that sublethal exposure to a neonicotinoid significantly reduces both mating success and sperm traits of male bumblebees. Sexually mature male Bombus terrestris exposed to a field-realistic concentration of thiamethoxam (20 ng g−1) or not (controls) were mated with virgin gynes in the laboratory. The results confirm sublethal negative effects of thiamethoxam on sperm quantity and viability. While the latency to mate was reduced, mating success was significantly impaired in thiamethoxam-exposed males by 32% probably due to female choice. Gynes mated by exposed males revealed impaired sperm traits compared to their respective controls, which may lead to severe constraints for colony fitness. Our laboratory findings demonstrate for the first time that neonicotinoid insecticides can negatively affect male mating success in bees. Given that holds true for the field, this provides a plausible mechanism contributing to declines of wild bee populations globally. The widespread prophylactic use of neonicotinoids may therefore have previously overlooked inadvertent anti-aphrodisiac effects on non-target animals, thereby limiting conservation efforts.

Cuckoo bumblebee males might reduce plant fitness

A recommendation of: Alessandro Fisogni, Gherardo Bogo, François Massol, Laura Bortolotti, Marta Galloni Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees https://doi.org/10.5281/zenodo.4489066

Alien balsams, strawberries and their pollinators in a warmer world

BackgroundStrawberries are a common crop whose yield success depends on the availability of pollinators. Invasive alien plants, such as Impatiens glandulifera and I. parviflora, are also attractive for bees and hoverflies, respectively, and occur in close proximity to strawberry cultivation areas. The aim of the study was to test whether alien plants may decrease pollination of strawberry cultivation. However, even if the pollinators are abundant, efficiency of their pollination may decrease as a result of revisits of flowers that were already probed. It is addressed by pollinators by scent marking. Moreover, such revisits can be determined by nectar replenishment, which may occur rapidly in nectar-rich flowers. We studied revisits to I. glandulifera by bumblebees and defined the factors that influence the probability of revisits (air temperature; pollinator species; family caste and size; flower area; sun radiation; and time of day).ResultsWe found that the two alien species decreased the number of pollinators visiting strawberries. Apoidea, Bombini and Syrphidae significantly decreased on Fragaria × ananassa when alien Impatiens were present. We also revealed the influence of increasing air temperature on bumblebee foraging, which was particularly significant for female workers. At very high temperatures (> 37°C), bumblebee males revisited probed flowers less often than female workers.ConclusionsOur results demonstrate that in experimental conditions attractive alien species decrease pollination of strawberries, which may negatively affect production of this crop. Although the results have not been verified in real-life strawberry fields yet, we recommend that alien plant species that share the same pollinators and occur in close proximity of strawberries are controlled. Moreover, we found that revisits of probed flowers may weaken feeding efficiency of bumblebees. If revisits are not induced by nectar replenishment, then global warming may pose a serious threat to the survival of colonies, which may have consequences also for the plants that attract them, e.g., for strawberries.

Flower strips enhance abundance of bumble bee queens and males in landscapes with few honey bee hives

Wild bee declines in agricultural landscapes have led farmers to supplement crops with honey bees. Simultaneously, environmental subsidy and conservation programmes have incentivized farmers to establish flower strips to support wild and managed pollinators. To find out if flower strips enhance, and competition from honey bees suppresses, wild bees in the landscape and across seasons, we surveyed bumble bee and honey bee abundances in 16 sites in Sweden in summer 2018. The centre of each site (2 km radius) was with or without an annual flower strip, and with or without added honey bee hives. We surveyed bees in each flower strip and in linear habitats in the landscape around each site, such as field edges and road verges. In the following spring, we surveyed bumble bee queen abundance in each site. We show that adding flower strips benefits bumble bee queen abundance the following year, but this effect is diminished if honeybee hives are added. In sites with flower strips, added honey bee hives reduced male bumble bee abundance. Our relatively small flower strip areas bolstered bumble bee population growth across seasons, probably by relieving a resource bottleneck. Adding honey bee hives in combination with flower strips to landscapes with few floral resources should be avoided as it cancelled the positive effect of flower strips.

Equivalent learning, but unequal participation: Male bumble bees learn comparably to females, but participate in cognitive assessments at lower rates

Sex-specific cognitive abilities are well documented. These can occur when sexes engage in different ecological contexts. Less known is whether different ecological contexts can also drive sex-specific participation rates in behavioral tests. Here, we explore this question in bumble bees, a group of eusocial insects where worker females and males exhibit stark socioecological differences. Among myriad colony maintenance tasks, workers forage for themselves and developing brood, while males forage only for themselves while mate-searching. Following upon previous studies suggesting no sex differences in bumble bee learning, we test the hypothesis that despite having equivalent associative learning abilities, males participate in cognitive assessments offering nutritional rewards at lower rates. Testing > 500 bees from nine colonies in a differential conditioning protocol, we find support for our hypothesis. An equivalent proportion of workers and males successfully completed our cognitive assessment, while a significantly lower proportion of males participated in the entire protocol. Unequal participation is a perennial issue in the behavioral sciences, limiting sample size and potentially biasing results. Our results suggest that to understand the true range of variation in cognition, sex-differences in participation must be accounted for.

Age-related mushroom body expansion in male sweat bees and bumble bees

A well-documented phenomenon among social insects is that brain changes occur prior to or at the onset of certain experiences, potentially serving to prime the brain for specific tasks. This insight comes almost exclusively from studies considering developmental maturation in females. As a result, it is unclear whether age-related brain plasticity is consistent across sexes, and to what extent developmental patterns differ. Using confocal microscopy and volumetric analyses, we investigated age-related brain changes coinciding with sexual maturation in the males of the facultatively eusocial sweat bee, Megalopta genalis, and the obligately eusocial bumble bee, Bombus impatiens. We compared volumetric measurements between newly eclosed and reproductively mature males kept isolated in the lab. We found expansion of the mushroom bodies—brain regions associated with learning and memory—with maturation, which were consistent across both species. This age-related plasticity may, therefore, play a functionally-relevant role in preparing male bees for mating, and suggests that developmentally-driven neural restructuring can occur in males, even in species where it is absent in females.

Dynamic Change of Gut Microbiota in the Male Bee of Bombus terrestris (Hymenoptera: Apidae)

The gut microbiota plays a key role in the development and health of bumble bees. Male bees are important for the reproductive activity of a colony, yet there are few studies on their gut microbiota. By using qPCR, we found that significant changes in total bacteria and six important bacteria genera from different developmental age points in males. And we compare the gut bacteria of male bees with workers. The results indicate that Gilliamella, Snodgrassella, and Lactobacillus are the dominant gut bacteria in male bees, which is consistent with the previous studies in worker bees, however, there are more total bacteria in male bees. Another gut bacteria genus, Bacillus may be a probiotic bacteria for reproduction in male bees, although the possible function of these bacteria require further study. This research can provide insight into the relationship between the bacterial community and the physiological health and reproductive capacity of male bumble bees.

Factors Influencing the Reproductive Ability of Male Bees: Current Knowledge and Further Directions.

Simple SummaryBumblebees and honeybees are well known as the dominant and most important pollinators in natural and agricultural ecosystems. The quality characteristics of their colonies depend greatly on the reproductive ability/quality of the parents (queens and drones). Male bees, despite their exclusive reproductive role and ability to determine colony quality, have been less considered than female bees, especially bumblebees. We reviewed the current studies on environmental factors and inherent characteristics that affect the mating success and fecundity of male honeybees and bumblebees. Temperature, nutrients, pesticides, body size, weight and age affect reproduction in male bees and consequently the progeny colony quality. However, more studies, especially in male bumblebees, are still needed to address the impacts of these factors in detail to confront the requirements of agricultural pollination and declining wild bee pollinators worldwide.Bumblebees and honeybees are very important pollinators and play a vital role in agricultural and natural ecosystems. The quality of their colonies is determined by the queens and the reproductive drones of mother colonies, and mated drones transmit semen, including half of the genetic materials, to queens and enhance their fertility. Therefore, factors affecting drone fecundity will also directly affect progeny at the colony level. Here, we review environmental and bee-related factors that are closely related to drone reproductive ability. The environmental factors that mainly affect the sperm count and the viability of males include temperature, nutrients and pesticides. In addition, the inherent characteristics of male bees, such as body size, weight, age, seminal fluid proteins and proteins of the spermathecal fluid, contribute to mating success, sperm quality during long-term storage in the spermathecae and the reproductive behaviors of queens. Based on the results of previous studies, we also suggest that the effects of somatotype dimorphism in bumblebee males on sperm quality and queen fecundity and the indispensable and exploitable function of gland proteins in the fecundity of males and queens should be given more attention in further studies.

No sex differences in learning in wild bumblebees

Abstract Females and males often face different sources of selection, resulting in dimorphism in morphological, physiological, and even cognitive traits. Sex differences are often studied in respect to spatial cognition, yet the different ecological roles of males and females might shape cognition in multiple ways. For example, in dietary generalist bumblebees (Bombus), the ability to learn associations is critical to female workers, who face informationally rich foraging scenarios as they collect nectar and pollen from thousands of flowers over a period of weeks to months to feed the colony. While male bumblebees likely need to learn associations as well, they only forage for themselves while searching for potential mates. It is thus less clear whether foraging males would benefit from the same associative learning performance as foraging females. In this system, as in others, cognitive performance is typically studied in lab-reared animals under captive conditions, which may not be representative of patterns in the wild. In the first test of sex and species differences in cognition using wild bumblebees, we compared the performance of Bombus vancouverensis nearcticus (formerly bifarius) and Bombus vosnesenskii of both sexes on an associative learning task at Sierra Nevada (CA) field sites. Across both species, we found that males and females did not differ in their ability to learn, although males were slower to respond to the sucrose reward. These results offer the first evidence from natural populations that male bumblebees may be equally as able to learn associations as females, supporting findings from captive colonies of commercial bees. The observed interspecific variation in learning ability opens the door to using the Bombus system to test hypotheses about comparative cognition.

Global effects of extreme temperatures on wild bumblebees.

Climate plays a key role in shaping population trends and determining the geographic distribution of species because of limits in species' thermal tolerance. An evaluation of species tolerance to temperature change can therefore help predict their potential spatial shifts and population trends triggered by ongoing global warming. We assessed inter- and intraspecific variations in heat resistance in relation to body mass, local mean temperatures, and evolutionary relationships in 39 bumblebee species, a major group of pollinators in temperate and cold ecosystems, across 3 continents, 6 biomes, and 20 regions (2386 male specimens). Based on experimental bioassays, we measured the time before heat stupor of bumblebee males at a heatwave temperature of 40°C. Interspecific variability was significant, in contrast to interpopulational variability, which was consistent with heat resistance being a species-specific trait. Moreover, cold-adapted species are much more sensitive to heat stress than temperate and Mediterranean species. Relative to their sensitivity to extreme temperatures, our results help explain recent population declines and range shifts in bumblebees following climate change.

Mating under climate change: Impact of simulated heatwaves on the reproduction of model pollinators

Abstract Climate change is related to an increase in frequency and intensity of extreme events such as heatwaves. It is well established that such events may worsen the current world‐wide biodiversity decline. In many organisms, heat stress is associated with direct physiological perturbations and could lead to a decrease of fitness. In contrast to endotherms, heat stress resistance has been poorly investigated in heterotherms; especially in insects, in which the internal physiological mechanisms available to regulate body temperature are almost negligible making them sensitive to extreme temperature variations. Wild bees are crucial pollinators for wild plants and crops. Among them, bumblebees are experiencing a strong decline across the world. Therefore, the ongoing global decline of these insect pollinators partly due to climate change could cause major economic issues. Here we assess how simulated heatwaves impact fertility and attractiveness (key parameters of sustainability) of bumblebee males. We used three model species: Bombus terrestris, a widespread and warm‐adapted species, B. magnus and B. jonellus, two declining and cold‐adapted species. We highlight that heat shock (40°C) negatively affects sperm viability and sperm DNA integrity only in the two cold‐adapted species. Heat shock can also impact the structure of cephalic labial glands and the production of pheromones only in the declining species. The specific disruption in key reproductive traits we identify following simulated heatwave conditions could provide one important mechanistic explanation for why some pollinators are in decline through climate change. A free Plain Language Summary can be found within the Supporting Information of this article.

The Importance of Males to Bumble Bee (Bombus Species) Nest Development and Colony Viability.

Simple SummaryPopulations of some bumble bee species have declined over the last decade. Recognizing the importance of bumble bees to agriculture and natural ecosystems, there has been an upwelling of research to better understand the underlying reasons for observed population declines. While most research has addressed the health of bumble bee females (i.e., workers and queens), males have been largely ignored. Here, we explore the available published literature on the role males play in improving queen health and reproductive fitness, as well as in overall nest success. We conclude that males serve a unique and important role in bumble bee colony success.Bumble bee population declines over the last decade have stimulated strong interest in determining causative factors and necessary conservation measures. Research attention has largely been directed toward bumble bee worker and queen health and their contributions to population stability, while male bees (i.e., drones) have typically been overlooked regarding their role in influencing colony fitness and longevity. In this review we assess existing literature on the diverse role of males within bumble bee nests and their importance to queen health and fitness, as well as to overall nest success. The implications of reproductive measures, including sperm transfer, mating behavior, mating plugs, and male immunity, among other topics, are examined. Overall, bumble bee males are found to drive colony function in a unique manner. Current knowledge gaps pertaining to the role of males are discussed. We highlight the importance of drones to queen success and fitness in many ways, and suggest future research exploring impacts of this often-neglected caste.