APIDOLOGIE

Metabolism and upper thermal limits of and
Kovac H, Käfer H, Stabentheiner A and Costa C
The Western honeybees and are closely related subspecies living in neighbouring regions. Metabolism and the upper lethal thermal limits are crucial physiological traits, adapted in the evolutionary process to environment and climate conditions. We investigated whether samples from these two ecotypes differ in these traits. The standard metabolic rate was higher in the population only at a high temperature (~40 °C; dVCO=12 nl s; <0.05), probably due to a higher body temperature (dT=1.5 °C; <0.01). The critical thermal maximum of activity and respiration was similar (difference activity CT=0.8 °C, respiratory CT=1.1 °C). The lethal temperature (LT, ) revealed higher tolerance and survival rates of the Ligustica bees (Carnica 50.3 °C; Ligustica 51.7 °C; <0.02). Results reveal the adaptation of the two subspecies to their historic climate conditions, possibly favouring Ligustica in a warming environment.
The Architecture of the Pollen Hoarding Syndrome in Honey Bees: Implications for Understanding Social Evolution, Behavioral Syndromes, and Selective Breeding
Rueppell O
Social evolution has influenced every aspect of contemporary honey bee biology, but the details are difficult to reconstruct. The reproductive ground plan hypothesis of social evolution proposes that central regulators of the gonotropic cycle of solitary insects have been coopted to coordinate social complexity in honey bees, such as the division of labor among workers. The predicted trait associations between reproductive physiology and social behavior have been identified in the context of the pollen hoarding syndrome, a larger suite of interrelated traits. The genetic architecture of this syndrome is characterized by a partially overlapping genetic architecture with several consistent, pleiotropic QTL. Despite these central QTL and an integrated hormonal regulation, separate aspects of the pollen hoarding syndrome may evolve independently due to peripheral QTL and additionally segregating genetic variance. The characterization of the pollen hoarding syndrome has also demonstrated that this syndrome involves many non-behavioral traits, which may be the case for numerous "behavioral" syndromes. Furthermore, the genetic architecture of the pollen hoarding syndrome has implications for breeding programs for improving honey health and other desirable traits: If these traits are comparable to the pollen hoarding syndrome, consistent pleiotropic QTL will enable marker assisted selection, while sufficient additional genetic variation may permit the dissociation of trade-offs for efficient multiple trait selection.
Contribution of honeybee drones of different age to colonial thermoregulation
Kovac H, Stabentheiner A and Brodschneider R
In addition to honeybee workers, drones also contribute to colonial thermoregulation. We show the drones' contribution to thermoregulation at 5 different experimental temperatures ranging from 15-34 °C. The frequency and the degree of endothermy depended on the drones' local ambient temperature and age. Location on brood or non-brood areas had no influence. The frequency of endothermic drones and the intensity of endothermy increased with decreasing temperature. 30% of drones of 8 days and older heated their thorax by more than 1 °C above the abdomen. The youngest drones (0-2 days) did not exceed this level of endothermy. Though young drones were less often engaged in active heat production, their contribution to brood warming was not insignificant because their abundance on the brood nest was 3.5 times higher than that of the oldest drones (≥13 days). Results suggest that the stimulus for the drones' increased frequency of heating at low experimental temperatures was their low local ambient air and/or comb temperature.
Immune responses of honeybees and their fitness costs as compared to bumblebees
Riessberger-Gallé U, Hernández López J, Schuehly W, Crockett S, Krainer S and Crailsheim K
Immune responses of invertebrates imply more than developing a merely unspecific response to an infection. Great interest has been raised to unveil whether this investment into immunity also involves fitness costs associated to the individual or the group. Focusing on the immune responses of honeybees, we use the well-studied insect bumblebee for comparison. Bumblebees are capable of producing specific immune responses to infections whereas this has not been assessed for honeybees so far. We investigated whether a prior bacterial encounter provides protection against a later exposure to the same or a different bacterium in honeybees. Additionally, we studied whether the foraging activities of honeybees and bumblebees are affected upon immune stimulation by assessing the flight performance. Finally, the acceptance behavior of nestmates toward immune-challenged honeybees was determined. Results show that despite stimulating the immune system of honeybees, no protective effects to infections were found. Further, honeybees were not affected by an immune challenge in their flight performance whereas bumblebees showed significant flight impairment. Immune-challenged honeybees showed lower survival rates than naive individuals when introduced into a regular colony. Here, we reveal different immune response-cost scenarios in honeybees and bumblebees for the first time.
Establishment risk of the commercially imported bumblebee -can they survive UK winters?
Owen EL, Bale JS and Hayward SA
Bumblebees are regularly exported to countries outside their native range for the purposes of commercial pollination. In contrast to the tight regulations imposed on biological control introductions, the movement of bumblebees has largely been without risk assessment. This study represents the first formal assessment of establishment risk for in the UK. The ability of workers to survive winter conditions is seen as the primary barrier to establishment, given the year-round colony activity of this sub-species. We use standardised cold tolerance indices as outlined by the EU policy support action 'REBECA' as well as assessing rapid cold hardening (RCH) ability. Cold tolerance was comparable to that of the UK-native , including a strong RCH response. Results suggest that could survive mild UK winters in southern areas and potentially displace . The implications of ongoing climate change on establishment risks are discussed.
Pathogen prevalence and abundance in honey bee colonies involved in almond pollination
Cavigli I, Daughenbaugh KF, Martin M, Lerch M, Banner K, Garcia E, Brutscher LM and Flenniken ML
Honey bees are important pollinators of agricultural crops. Since 2006, US beekeepers have experienced high annual honey bee colony losses, which may be attributed to multiple abiotic and biotic factors, including pathogens. However, the relative importance of these factors has not been fully elucidated. To identify the most prevalent pathogens and investigate the relationship between colony strength and health, we assessed pathogen occurrence, prevalence, and abundance in Western US honey bee colonies involved in almond pollination. The most prevalent pathogens were Black queen cell virus (BQCV), Lake Sinai virus 2 (LSV2), Sacbrood virus (SBV), , and trypanosomatids. Our results indicated that pathogen prevalence and abundance were associated with both sampling date and beekeeping operation, that prevalence was highest in honey bee samples obtained immediately after almond pollination, and that weak colonies had a greater mean pathogen prevalence than strong colonies.
Distance Between Honey Bee Colonies Regulates Populations of at a Landscape Scale
Nolan MP and Delaplane KS
Inter-colony distance of significantly affects colony numbers of the parasitic mite . We set up 15 apiaries, each consisting of two colonies. Each apiary pair was assigned an inter-colony distance of 0, 10, or 100 m. Colonies were rendered nearly mite-free, then one colony in each pair was seeded with 300 female mites (mite-donor colony), while the other remained uninoculated (mite-recipient colony). After four months of monitoring, a whole model analysis showed that apiaries in which colonies were spaced 100 m apart contained lower average mite numbers than 0 m or 10 m apiaries. There were interactions among colony type, distance, and sampling date; however, when there were significant differences mite numbers were always lower in 100 m apiaries than 10 m apiaries. These findings pose the possibility that Varroa populations are resource regulated at a landscape scale: near-neighbor colonies constitute reproductive resource for mites in the form of additional bee brood.
Fine scale population genetic structure of , an ectoparasitic mite of the honey bee ()
Dynes TL, De Roode JC, Lyons JI, Berry JA, Delaplane KS and Brosi BJ
is an obligate ectoparasitic mite and the most important biotic threat currently facing honey bees (). We used neutral microsatellites to analyze previously unreported fine scale population structure of , a species characterized by extreme lack of genetic diversity owing to multiple bottleneck events, haplodiploidy, and primarily brother-sister matings. Our results surprisingly indicate that detectable hierarchical genetic variation exists between apiaries, between colonies within an apiary, and even within colonies. This finding of within-colony parasite diversity provides empirical evidence that the spread of is not accomplished solely by vertical transmission but that horizontal transmission (natural or human-mediated) must occur regularly.
Nuclear translocation of vitellogenin in the honey bee ()
Salmela H, Harwood GP, Münch D, Elsik CG, Herrero-Galán E, Vartiainen MK and Amdam GV
Vitellogenin (Vg) is a conserved protein used by nearly all oviparous animals to produce eggs. It is also pleiotropic and performs functions in oxidative stress resistance, immunity, and, in honey bees, behavioral development of the worker caste. It has remained enigmatic how Vg affects multiple traits. Here, we asked whether Vg enters the nucleus and acts via DNA-binding. We used cell fractionation, immunohistology, and cell culture to show that a structural subunit of honey bee Vg translocates into cell nuclei. We then demonstrated Vg-DNA binding theoretically and empirically with prediction software and chromatin immunoprecipitation with sequencing (ChIP-seq), finding binding sites at genes influencing immunity and behavior. Finally, we investigated the immunological and enzymatic conditions affecting Vg cleavage and nuclear translocation and constructed a 3D structural model. Our data are the first to show Vg in the nucleus and suggest a new fundamental regulatory role for this ubiquitous protein.
50 years
Courant C, Koeniger G and Hartfelder K
Since its foundation, has steadily gained recognition as a journal that reports results from high-quality scientific research on the biology of bees, and this means Apidae in general, not only on its most prominent species, the Western honey bee, . All started 50 years ago in a conversation between two eminent scientists, Jean Louveaux, director of one of INRA's bee research unit in Bures-sur-Yvette and editor of the French , and Friedrich Ruttner, director of the Bee Research Institute in Oberursel and editor of the German , where they discussed the possibility of merging these two journals to create an international bee research journal. Here, we take 's 50th anniversary as an opportunity to provide our readers with background information on the journal's history, especially on the persons and their contributions along this journey.
Urbanisation is associated with reduced sp. infection, higher colony strength and higher richness of foraged pollen in honeybees
Samuelson AE, Gill RJ and Leadbeater E
Bees are vital pollinators, but are faced with numerous threats that include loss of floral resources and emerging parasites amongst others. Urbanisation is a rapidly expanding driver of land-use change that may interact with these two major threats to bees. Here we investigated effects of urbanisation on food store quality and colony health in honeybees () by sampling 51 hives in four different land-use categories: urban, suburban, rural open and rural wooded during two seasons (spring and autumn). We found positive effects of urban land use on colony strength and richness of stored pollen morphotypes, alongside lower late-season sp. infection in urban and suburban colonies. Our results reveal that honeybees exhibit lower colony performance in strength in rural areas, adding to the growing evidence that modern agricultural landscapes can constitute poor habitat for insect pollinators.
Overview of the testing and assessment of effects of microbial pesticides on bees: strengths, challenges and perspectives
Borges S, Alkassab AT, Collison E, Hinarejos S, Jones B, McVey E, Roessink I, Steeger T, Sultan M and Wassenberg J
Currently, there is a growing interest in developing biopesticides and increasing their share in the plant protection market as sustainable tools in integrated pest management (IPM). Therefore, it is important that regulatory requirements are consistent and thorough in consideration of biopesticides' unique properties. While microbial pesticides generally have a lower risk profile, they present special challenges in non-target organism testing and risk assessment since, in contrast to chemical pesticides, their modes of action include infectivity and pathogenicity rather than toxicity alone. For this reason, non-target organism testing guidelines designed for conventional chemical pesticides are not necessarily directly applicable to microbial pesticides. Many stakeholders have recognised the need for improvements in the guidance available for testing microbial pesticides with honey bees, particularly given the increasing interest in development and registration of microbial pesticides and concerns over risks to pollinators. This paper provides an overview of the challenges with testing and assessment of the effects of microbial pesticides on honey bees (), which have served as a surrogate for both and non- bees, and provides a foundation toward developing improved testing methods.
How diverse is the chemistry and plant origin of Brazilian propolis?
Salatino A, Salatino MLF and Negri G
Propolis is a honey bee product containing chiefly beeswax and resins originated from plant buds or exudates. Propolis resin exerts a diversity of biological activities, such as antitumoral, anti-inflammatory, antimicrobial, and defense of the hive against pathogens. Chemical standardization and identification of botanical sources is crucial for characterization of propolis. Types of Brazilian propolis are characteristic of geographical regions and respective biomes, such as savannas (Cerrado), mangroves, dry forest (Caatinga), rain forests (Amazon, Atlantic, and Interior forests), altitudinal fields ("Campos Rupestres"), Pantanal, and forests. Despite the wide diversity of Brazilian biomes and flora, relatively few types of Brazilian propolis and corresponding resin plant sources have been reported. Factors accounting for the restricted number of known types of Brazilian propolis and plant sources are tentatively pointed out. Among them, the paper discusses constraints that honey bees must overcome to collect plant exudates, including the characteristics of the lapping-chewing mouthpart of honey bee, which limit their possibilities to cut and chew plant tissues, as well as chemical requirements that plant resins must fulfil, involving antimicrobial activity of its constituents and innocuity to the insects. Although much still needs to be done toward a more comprehensive picture of Brazilian propolis types and corresponding plant origins, the prospects indicate that the actual diversity of plant sources of honey bee propolis will remain relatively low.
Charles Henry Turner and the cognitive behavior of bees
Giurfa M, de Brito AG, de Brito TG and de Brito Sanchez MG
Social movements in several countries are stimulating a reconsideration of academic structures and historic figures and promoting reparation and recognition of marginalized and forgotten black scientists. A paradigmatic case in that sense is Charles Henry Turner (1867-1923) who was the first African American to receive a graduate degree at the University of Cincinnati and one of the first in earning a PhD degree of the University of Chicago. He performed numerous experiments on sensory perception, orientation, and mating of solitary and social bees, most of which have been unjustly forgotten despite the fact that they anticipated fundamental concepts of animal cognition. We review these studies and highlight the importance of his ideas for modern views of animal cognition and the study of bee behavior. We conclude that besides his scientific contributions, Turner is an inspiration for scientists fighting against social adversity and prejudices.
Lower pollen nutritional quality delays nest building and egg laying in micro-colonies leading to reduced biomass gain
Ryder JT, Cherrill A, Thompson HM and Walters KFA
The performance of micro-colonies fed five diets differing in pollen species composition and level of nine essential amino acids (EAA; leucine, lysine, valine, arginine, isoleucine, phenylalanine, threonine, histidine, methionine) was assessed for 37 days by recording total biomass gain, nest building initiation, brood production (eggs, small and large larvae, pupae, drones), nectar, and pollen collection. Stronger colony performance was linked to higher amino acid levels but no consistent differences in biomass gain were recorded between mono- and poly-species diets. Poorest performance occurred in micro-colonies offered pure oilseed rape (OSR) pollen which contained the lowest EAA levels. Reduced micro-colony development (delayed nest initiation and lower brood production) was related to OSR proportion in the diet and lower EAA levels. Results are discussed in relation to selection of plant species in the design of habitats to promote bee populations.
A gene drive does not spread easily in populations of the honey bee parasite
Faber NR, Meiborg AB, Mcfarlane GR, Gorjanc G and Harpur BA
Varroa mites () are the most significant threat to beekeeping worldwide. They are directly or indirectly responsible for millions of colony losses each year. Beekeepers are somewhat able to control varroa populations through the use of physical and chemical treatments. However, these methods range in effectiveness, can harm honey bees, can be physically demanding on the beekeeper, and do not always provide complete protection from varroa. More importantly, in some populations varroa mites have developed resistance to available acaricides. Overcoming the varroa mite problem will require novel and targeted treatment options. Here, we explore the potential of gene drive technology to control varroa. We show that spreading a neutral gene drive in varroa is possible but requires specific colony-level management practices to overcome the challenges of both inbreeding and haplodiploidy. Furthermore, continued treatment with acaricides is necessary to give a gene drive time to fix in the varroa population. Unfortunately, a gene drive that impacts female or male fertility does not spread in varroa. Therefore, we suggest that the most promising way forward is to use a gene drive which carries a toxin precursor or removes acaricide resistance alleles.
Assessing virulence of mites from different honey bee management regimes
Dynes TL, Berry JA, Delaplane KS, de Roode JC and Brosi BJ
The mite is an important honey bee parasite that causes substantial losses of honey bee colonies worldwide. Evolutionary theory suggests that the high densities at which honey bees are managed in large-scale beekeeping settings will likely select for mites with greater growth and virulence, thereby potentially explaining the major damage done by these mites. We tested this hypothesis by collecting mites from feral bee colonies, "lightly" managed colonies (those from small-scale sedentary operations), and "heavily" managed colonies (those from large-scale operations that move thousands of colonies across the US on a yearly basis). We established 8 apiaries, each consisting of 11 colonies from a standardized lightly managed bee background that were cleared of mites, and artificially infested each apiary with controlled numbers of mites from feral, lightly managed, or heavily managed bees or left uninoculated as negative control. We monitored the colonies for more than 2 years for mite levels, colony strength (adult bee population, brood coverage, and honey storage), and survival. As predicted by evolutionary theory, we found that colonies inoculated with mites from managed backgrounds had increased mite levels relative to those with mites from feral colonies or negative controls. However, we did not see a difference between heavily and lightly managed colonies, and these higher mite burdens did not translate into greater virulence, as measured by reductions in colony strength and survival. Our results suggest that human management of honey bee colonies may favor the increased population growth rate of , but that a range of potential confounders (including viral infections and genotype-by-genotype interactions) likely contribute to the relationship between mite reproduction and virulence.
The effects of diet enhancement on the health of commercial bumblebee colonies
Hulse RA, Van Oystaeyen A, Carnell JD, Beckett D, Grey WG, Goulson D, Wackers F and Hughes WOH
Commercially reared bees provide economically important pollination services for a diversity of crops. Improving their health is important both to maximise their pollination services and to avoid possible pathogen spillover or spillback with wild pollinators. Diet quality may directly or indirectly affect diverse aspects of bumblebee health, including colony development, individual size and immune health, but the impact of this remains unclear. Here we investigate experimentally the effect of diet quality during bumblebee colony development using three diets: (1) a standard pollen diet used in commercial rearing of colonies for sale, (2) an enhanced diet comprised of a wildflower pollen mix that was expected to be nutritionally superior (including by having an elevated protein content) and (3) a diet of pollen substitute mixed with the standard diet that was expected to be nutritionally poorer. The effect of diet quality on colony health was quantified using colony-level measures (colony weight, size [number of live workers] and number of dead individuals), and individual-level measures (body size, fat body size [proportion of body weight], total haemocyte count and phenoloxidase immune enzyme activity). Diet quality significantly affected colony growth, with colonies fed the enhanced diet growing larger and producing more reproductives than those fed either a standard or poor diet. The enhanced diet also resulted in bees that were significantly larger and had better immune health. The results show that diet can have important effects on the health of commercially reared bumblebees and suggest that the enhancement of standard-rearing diets may improve colony health.