Reproduction of Varroa destructor in worker brood of Africanized honey bees (Apis mellifera)

Reproduction and population growth of Varroa destructor was studied in ten naturally infested, Africanized honeybee (AHB) (Apis mellifera) colonies in Yucatan, Mexico. Between February 1997 and January 1998 monthly records of the amount of pollen, honey, sealed worker and drone brood were recorded. In addition, mite infestation levels of adult bees and worker brood and the fecundity of the mites reproducing in worker cells were determined. The mean number of sealed worker brood cells (10,070 ± 1,790) remained fairly constant over the experimental period in each colony. However, the presence and amount of sealed drone brood was very variable. One colony had drone brood for 10 months and another for only 1 month. Both the mean infestation level of worker brood (18.1 ± 8.4%) and adult bees (3.5 ± 1.3%) remained fairly constant over the study period and did not increase rapidly as is normally observed in European honey bees. In fact, the estimated mean number of mites fell from 3,500 in February 1997 to 2,380 in January 1998. In May 2000 the mean mite population in the study colonies was still only 1,821 mites. The fertility level of mites in this study was much higher (83–96%) than in AHB in Brazil(25–57%), and similar to that found in EHB (76–94%). Mite fertility remained high throughout the entire study and was not influenced by the amount of pollen, honey or worker brood in the colonies. This revised version was published online in July 2006 with corrections to the Cover Date.     

Effects of Imidacloprid and Varroa destructor on survival and health of European honey bees,Apis mellifera

There has been growing concern over declines in populations of honey bees and other pollinators which are a vital part to our food security. It is imperative to identify factors responsible for accelerated declines in bee populations and develop solutions for reversing bee losses. While exact causes of colony losses remain elusive, risk factors thought to play key roles are ectoparasitic mites Varroa destructor and neonicotinoid pesticides. The present study aims to investigate effects of a neonicotinoid pesticide Imidacloprid and Varroa mites individually on survivorship, growth, physiology, virus dynamics and immunity of honey bee workers. Our study provides clear evidence that the exposure to sublethal doses of Imidacloprid could exert a significantly negative effect on health and survival of honey bees. We observed a significant reduction in the titer of vitellogenin (Vg), an egg yolk precursor that regulates the honey bees development and behavior and often are linked to energy homeostasis, in bees exposed to Imidacloprid. This result indicates that sublethal exposure to neonicotinoid could lead to increased energy usage in honey bees as detoxification is a energy‐consuming metabolic process and suggests that Vg could be a useful biomarker for measuring levels of energy stress and sublethal effects of pesticides on honey bees. Measurement of the quantitative effects of different levels of Varroa mite infestation on the replication dynamic of Deformed wing virus (DWV), an RNA virus associated with Varroa infestation, and expression level of immune genes yields unique insights into how honey bees respond to stressors under laboratory conditions.     

Unique features of flight muscles mitochondria of honey bees (Apis mellifera L.)

Honey bees Apis mellifera L. are one of the most studied insect species due to their economic importance. The interest in studying honey bees chiefly stems from the recent rapid decrease in their world population, which has become a problem of food security. Nevertheless, there are no systemic studies on the properties of the mitochondria of honey bee flight muscles. We conducted a research of the mitochondria of the flight muscles of A. mellifera L. The influence of various organic substrates on mitochondrial respiration in the presence or absence of adenosine diphosphate (ADP) was investigated. We demonstrated that pyruvate is the optimal substrate for the coupled respiration. A combination of pyruvate and glutamate is required for the maximal respiration rate. We also show that succinate oxidation does not support the oxidative phosphorylation and the generation of membrane potential. We also studied the production of reactive oxygen species by isolated mitochondria. The greatest production of H₂O₂ (as a percentage of the rate of oxygen consumed) in the absence of ADP was observed during the respiration supported by α‐glycerophosphate, malate, and a combination of malate with another NAD‐linked substrate. We showed that honey bee flight muscle mitochondria are unable to uptake Ca²⁺‐ions. We also show that bee mitochondria are able to oxidize the respiration substrates effectively at the temperature of 50°С compared to Bombus terrestris mitochondria, which were more adapted to lower temperatures.     

Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor

Varroa destructor is a highly virulent ectoparasitic mite of the honey bee Apis mellifera and a major cause of colony losses for global apiculture. Typically, chemical treatment is essential to control the parasite population in the honey bee colony. Nevertheless a few honey bee populations survive mite infestation without any treatment. We used one such Varroa mite tolerant honey bee lineage from the island of Gotland, Sweden, to identify quantitative trait loci (QTL) controlling reduced mite reproduction. We crossed a queen from this tolerant population with drones from susceptible colonies to rear hybrid queens. Two hybrid queens were used to produce a mapping population of haploid drones. We discriminated drone pupae with and without mite reproduction, and screened the genome for potential QTL using a total of 216 heterozygous microsatellite markers in a bulk segregant analysis. Subsequently, we fine mapped three candidate target regions on chromosomes 4, 7, and 9. Although the individual effect of these three QTL was found to be relatively small, the set of all three had significant impact on suppression of V. destructor reproduction by epistasis. Although it is in principle possible to use these loci for marker-assisted selection, the strong epistatic effects between the three loci complicate selective breeding programs with the Gotland Varroa tolerant honey bee stock.     

Changes in the reproductive ability of the mite Varroa destructor (Anderson e Trueman) in africanized honey bees (Apis mellifera L.) (Hymenoptera: Apidae) colonies in southern Brazil

Varroa destructor has been in Brazil for more than 30 years, but no mortality of honeybee colonies due to this mite has been recorded. Africanized bee infestation rates attained by varroa have been low, without causing measurable damage to Brazilian apiculture. The low reproductive ability of this parasite in Africanized bee worker brood cells has been considered an important factor for maintaining the host-parasite equilibrium. Nevertheless, the possible substitution of the haplotype of the mite Varroa destructor that has occurred recently in Brazil could affected the reproductive ability of the population of this parasite in Brazil. The reproductive ability of worker of the mite females was evaluated in over one thousand 17-18 day-old Africanized worker brood cells each of the two periods. The percentage of fertile mites increased from 56% in the 1980s to 86% in 2005-2006. The difference in the percentage of females that produced deutonymphs, female progeny that can reach the adult stage at bee emergence, was even greater. In 2005-2006, 72% of the females that invaded worker brood had left at the least one viable descendant, compared to 35% in 1986-1987.     

Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.)

Using the proboscis extension response we conditioned pollen and nectar foragers of the honey bee (Apis mellifera L.) to tactile patterns under laboratory conditions. Pollen foragers demonstrated better acquisition, extinction, and reversal learning than nectar foragers. We tested whether the known differences in response thresholds to sucrose between pollen and nectar foragers could explain the observed differences in learning and found that nectar foragers with low response thresholds performed better during acquisition and extinction than ones with higher thresholds. Conditioning pollen and nectar foragers with similar response thresholds did not yield differences in their learning performance. These results suggest that differences in the learning performance of pollen and nectar foragers are a consequence of differences in their perception of sucrose. Furthermore, we analysed the effect which the perception of sucrose reward has on associative learning. Nectar foragers with uniform low response thresholds were conditioned using varying concentrations of sucrose. We found significant positive correlations between the concentrations of the sucrose rewards and the performance during acquisition and extinction. The results are summarised in a model which describes the relationships between learning performance, response threshold to sucrose, concentration of sucrose and the number of rewards. Accepted: 14 April 1999     

Nosema ceranae in European honey bees (Apis mellifera)

Nosema ceranae is a microsporidian parasite described from the Asian honey bee, Apis cerana. The parasite is cross-infective with the European honey bee, Apis mellifera. It is not known when or where N. ceranae first infected European bees, but N. ceranae has probably been infecting European bees for at least two decades. N. ceranae appears to be replacing Nosema apis, at least in some populations of European honey bees. This replacement is an enigma because the spores of the new parasite are less durable than those of N. apis. Virulence data at both the individual bee and at the colony level are conflicting possibly because the impact of this parasite differs in different environments. The recent advancements in N. ceranae genetics, with a draft assembly of the N. ceranae genome available, are discussed and the need for increased research on the impacts of this parasite on European honey bees is emphasized.     

Nosema ceranae in drone honey bees (Apis mellifera)

Nosema ceranae is a microsporidian intracellular parasite of honey bees, Apis mellifera. Previously Nosema apis was thought to be the only cause of nosemosis, but it has recently been proposed that N. ceranae is displacing N. apis. The rapid spread of N. ceranae could be due to additional transmission mechanisms, as well as higher infectivity. We analyzed drones for N. ceranae infections using duplex qPCR with species specific primers and probes. We found that both immature and mature drones are infected with N. ceranae at low levels. This is the first report detecting N. ceranae in immature bees. Our data suggest that because drones are known to drift from their parent hives to other hives, they could provide a means for disease spread within and between apiaries.     

Genotypic variability and relationships between mite infestation levels, mite damage, grooming intensity, and removal of Varroa destructor mites in selected strains of worker honey bees (Apis mellifera L.)

The objective of this study was to demonstrate genotypic variability and analyze the relationships between the infestation levels of the parasitic mite Varroa destructor in honey bee (Apis mellifera) colonies, the rate of damage of fallen mites, and the intensity with which bees of different genotypes groom themselves to remove mites from their bodies. Sets of paired genotypes that are presumably susceptible and resistant to the varroa mite were compared at the colony level for number of mites falling on sticky papers and for proportion of damaged mites. They were also compared at the individual level for intensity of grooming and mite removal success. Bees from the "resistant" colonies had lower mite population rates (up to 15 fold) and higher percentages of damaged mites (up to 9 fold) than bees from the "susceptible" genotypes. At the individual level, bees from the "resistant" genotypes performed significantly more instances of intense grooming (up to 4 fold), and a significantly higher number of mites were dislodged from the bees' bodies by intense grooming than by light grooming (up to 7 fold) in all genotypes. The odds of mite removal were high and significant for all "resistant" genotypes when compared with the "susceptible" genotypes. The results of this study strongly suggest that grooming behavior and the intensity with which bees perform it, is an important component in the resistance of some honey bee genotypes to the growth of varroa mite populations. The implications of these results are discussed.     

Nurse bees support the physiological development of young bees (Apis mellifera L.)

Newly emerged worker honeybees (focal bees) were caged individually for 8 days either isolated or together with one companion bee of known age (2–30 days) taken from a colony. The companion bee was replaced every 2nd day. After 8 days, various parameters were investigated in the focal bees as indicators of the level of development. Focal bees which had been caged with 6-day-old companion bees were better developed than isolated focal bees, newly emerged bees, or focal bees caged with almost all other ages of companion bees. They had hypopharyngeal glands that were larger and contained more protein, their thoraces had a higher protein content, and they had a higher rate of proteolytic activity in the midgut. Although the focal bees were supplied with pollen as well as honey, they consumed only small amounts of pollen. We attribute their better development to their having been fed worker jelly by the accompanying companion bees. The 6-day-old companion bees consumed high quantities of pollen and spent more time (18.7 ± 11.85 s/h) feeding focal bees than 12-day-old bees (6.5 ± 4.09 s/h) or foragers (no feeding of focal bees). The results show that even under such artificial conditions, the exchange of food (trophallaxis) promotes the development of young honeybee workers. Accepted: 26 February 1999     

Thermoregulation of water collecting honey bees (Apis mellifera)

Honey bees (Apis mellifera carnica, Apidae, Hymenoptera) visited a pond in order to collect water. During their stays at the pond the body surface temperature of water foragers was measured using contactless thermography. Irrespective of the ambient temperature (T(A)) which ranged from 13.6 to 27.2 degrees C, the water carriers reached thoracic temperatures of 36-38.8 degrees C (mean values of the measuring periods). The maximum thoracic value of an individual bee was 44.5 degrees C. At higher T(A) (20.9-27.2 degrees C) head and abdomen were only about 3 degrees C and 2 degrees C on the average higher than the surroundings, respectively. In the lower range of T(A) (13.6-16.6 degrees C), however, the bees warmed their heads up to 29.2 degrees C (13 degrees C above T(A)) and the abdomen up to 23.3 degrees C (7.1 degrees C above T(A); mean values of the measuring periods).The head and abdomen were even provided independently of one another with heat from the thorax. At a higher T(A) only little heat came from the heated thorax into the abdomen, at a cooler T(A) (13.6-16.6 degrees C) more heat reached the abdomen. In all probability, at a higher T(A) only a small amount of haemolymph was pumped from the thorax into the abdomen; the most warm blood probably circulated in the head-thorax area. The average duration of stays at the pond decreased linearly from 110 to 42 s with rising T(A). Head and thorax showed great fluctuations of temperature. For example, the head was heated by 4.6 degrees C within 25 s, the thorax by 6.1 degrees C within 30 s.Foragers drinking sucrose solution are known to increase their thoracic temperature with rising concentration of the sucrose solution. The water foragers had thoracic temperatures similar to that of bees feeding on 0.5 molar sucrose solution. It is hypothesized that the foraging motivation of both groups was similar and therefore they regulated their thoraces at the same temperature level.     

A modeling approach to swarming in honey bees (Apis mellifera)

Identifying the mechanisms of colony reproduction is essential to understanding the sociobiology of honey bees. Although several proximate causes leading to the initiation of queen rearing – an essential prerequisite to swarming – have been proposed, none have received unequivocal empirical support. Here we model the main proximate hypotheses (colony size, brood comb congestion, and worker age distribution) and show that all proposed swarming triggers occur as a function of the ultimate cause of a colony reaching replacement stability, the point at which the queen has been laying eggs at her maximal rate. We thus present a reproductive optimization model of colony swarming based on evolutionary principles. All models produce results remarkably similar both to each other and to empirically-determined swarming patterns. An examination of the fit between the individual models and swarm-preventing techniques used by beekeepers indicates that the reproductive optimization model has a relatively broad explanatory range. These results suggest that an examination into the behavioral correlates of a queen’s maximum egg laying rate may provide a unified proximate mechanistic trigger leading predictably to colony fission. Generating a predictive model for this very well studied animal is the first step in producing a model of colony fission applicable to other swarm-founding eusocial animals. Received 16 November 2004; revised 31 May 2005; accepted 27 June 2005.     

Group relatedness and kin discrimination in honey bees Apis mellifera L.

In addressing problems concerning kin discrimination and the evolutionary significance of inclusive fitness in highly eusocial insects, the genetic relatedness between groups, such as individuals belonging to the same patriline within colonies, is of interest. Based on the definitions for individual genetic relationship, several new measurements of group relatedness are derived and their genetical meaning is discussed. In a metabolic bioassay for the documentation of kin discrimination, carbon dioxide production was used to quantify reactions of groups of honey bees to volatile odours of other groups. Worker test groups, which had not experienced their hive environment, were able to discriminate between related and unrelated groups of workers within and between colonies. Test groups responded in a similar way to odours of genotypically mixed groups with related and unrelated workers and to the odours of pure groups of the less related subgroup. Thus, the reaction to group odours that function as discrimination labeles is not a linear response as predicted by an additive gestalt odour model. Since experienced bees collected from the colony could not discriminate between the various patrilines, the observed phenomenon resembles nest mate recognition rather than within-colony kin recognition.