Hasan Al Toufailia

Towards integrated control of varroa: effect of variation in hygienic behaviour among honey bee colonies on mite population increase and deformed wing virus incidence

Summary Hygienic behaviour in the honey bee, Apis mellifera, is the uncapping and removal of dead, diseased or infected brood from sealed cells by worker bees. We determined the effect of hygienic behaviour on varroa population growth and incidence of deformed wing virus (DWV), which can be transmitted by varroa. We treated 42 broodless honey bee colonies with oxalic acid in early January 2013 to reduce varroa populations to low levels, which we quantified by extracting mites from a sample of worker bees. We quantified varroa levels, again when the colonies were broodless, 48 weeks later. During the summer the hygienic behaviour in each colony was quantified four times using the Freeze Killed Brood (FKB) removal assay, and ranged from 27.5% to 100%. Varroa population increased greatly over the season, and there was a significant negative correlation between varroa increase and FKB removal. This was entirely due to fully hygienic colonies with > 95% FKB having only 43% of the varroa build up of the less hygienic colonies. None of the 14 colonies with >80 % FKB removal had overt symptoms of DWV, whilst 36% of the less hygienic colonies did. Higher levels of FKB removal also correlated significantly with lower numbers of DWV RNA copies in worker bees, but not in varroa mites. On average, fully hygienic colonies had c. 10,000 times less viral RNA than less hygienic colonies.

Towards integrated control of varroa: 2)comparing application methods and doses of oxalic acid on the mortality of phoretic Varroa destructor mites and their honey bee hosts

In the past two decades, the parasitic mite Varroa destructor has become harder to control with synthetic acaricide chemicals due to genetic resistance. We determined the efficacy of the natural chemical oxalic acid (OA) in killing phoretic mites on adult worker bees under field conditions in southern England. We compared three OA application methods (trickling, spraying, and sublimation) at three or four (sublimation) doses, using 110 broodless colonies in early January 2013. Treatment efficacy was assessed by extracting mites from samples of c. 270 worker bees collected immediately before and 10 days after treatment. All three methods could give high varroa mortality, c. 93–95%, using 2.25 g OA per colony. However, sublimation was superior as it gave higher mortality at lower doses (.56 or 1.125 g per colony: trickling 20, 57% mortality; spraying 25, 86%; sublimation 81, 97%.). Sublimation using 2.25 g of OA also resulted in 3 and 12 times less worker bee mortality in the 10 days after application than either trickling or spraying, respectively, and lower colony mortality four months later in mid spring. Colonies treated via sublimation also had greater brood area four months later than colonies treated via trickling, spraying, or control colonies. A second trial in December 2013 treated 89 broodless colonies with 2.25 g OA via sublimation to confirm the previous results. Varroa mortality was 97.6% and 87 (98%) of the colonies survived until spring. This confirms that applying OA via sublimation in broodless honey bee colonies in winter is a highly effective way of controlling V. destructor and causes no harm to the colonies.

Caffeinated Forage Tricks Honeybees into Increasing Foraging and Recruitment Behaviors

In pollination, plants provide food reward to pollinators who in turn enhance plant reproduction by transferring pollen, making the relationship largely cooperative; however, because the interests of plants and pollinators do not always align, there exists the potential for conflict, where it may benefit both to cheat the other [1, 2]. Plants may even resort to chemistry: caffeine, a naturally occurring, bitter-tasting, pharmacologically active secondary compound whose main purpose is to detract herbivores, is also found in lower concentrations in the nectar of some plants, even though nectar, unlike leaves, is made to be consumed by pollinators. [corrected]. A recent laboratory study showed that caffeine may lead to efficient and effective foraging by aiding honeybee memory of a learned olfactory association [4], suggesting that caffeine may enhance bee reward perception. However, without field data, the wider ecological significance of caffeinated nectar remains difficult to interpret. Here we demonstrate in the field that caffeine generates significant individual- and colony-level effects in free-flying worker honeybees. Compared to a control, a sucrose solution with field-realistic doses of caffeine caused honeybees to significantly increase their foraging frequency, waggle dancing probability and frequency, and persistency and specificity to the forage location, resulting in a quadrupling of colony-level recruitment. An agent-based model also demonstrates how caffeine-enhanced foraging may reduce honey storage. Overall, caffeine causes bees to overestimate forage quality, tempting the colony into sub-optimal foraging strategies, which makes the relationship between pollinator and plant less mutualistic and more exploitative. VIDEO ABSTRACT.In pollination, plants provide food reward to pollinators who in turn enhance plant reproduction by transferring pollen, making the relationship largely cooperative; however, because the interests of plants and pollinators do not always align, there exists the potential for conflict, where it may benefit both to cheat the other [1, 2]. Plants may even resort to chemistry: caffeine, a naturally occurring, bitter-tasting, pharmacologically active secondary compound whose main purpose is to detract herbivores, is also found in lower concentrations in the nectar of some plants, even though nectar, unlike leaves, is made to be consumed by pollinators. [corrected]. A recent laboratory study showed that caffeine may lead to efficient and effective foraging by aiding honeybee memory of a learned olfactory association [4], suggesting that caffeine may enhance bee reward perception. However, without field data, the wider ecological significance of caffeinated nectar remains difficult to interpret. Here we demonstrate in the field that caffeine generates significant individual- and colony-level effects in free-flying worker honeybees. Compared to a control, a sucrose solution with field-realistic doses of caffeine caused honeybees to significantly increase their foraging frequency, waggle dancing probability and frequency, and persistency and specificity to the forage location, resulting in a quadrupling of colony-level recruitment. An agent-based model also demonstrates how caffeine-enhanced foraging may reduce honey storage. Overall, caffeine causes bees to overestimate forage quality, tempting the colony into sub-optimal foraging strategies, which makes the relationship between pollinator and plant less mutualistic and more exploitative. VIDEO ABSTRACT.

Honey bee waggle dance communication: signal meaning and signal noise affect dance follower behaviour

Returning honey bee foragers perform waggle dances to inform nestmate foragers about the presence, location and odour of profitable food sources and new nest sites. The aim of this study is to investigate how the characteristics of waggle dances for natural food sources and environmental factors affect dance follower behaviour. Because food source profitability tends to decrease with increasing foraging distance, we hypothesised that the attractiveness of a dance, measured as the number of dance followers and their attendance, decreases with increasing distance to the advertised food location. Additionally, we determined whether time of year and dance signal noise, quantified as the variation in waggle run direction and duration, affect dance follower behaviour. Our results suggest that bees follow fewer waggle runs as the food source distance increases, but that they invest more time in following each dance. This is because waggle run duration increases with increasing foraging distance. Followers responded to increased angular noise in dances indicating more distant food sources by following more waggle runs per dance than when angular noise was low. The number of dance followers per dancing bee was also affected by the time of year and varied among colonies. Our results provide evidence that both noise in the message, that is variation in the direction component, and the message itself, that is the distance of the advertised food location, affect dance following. These results indicate that dance followers may pay attention to the costs and benefits associated with using dance information.

The effect of one generation of controlled mating on the expression of hygienic behaviour in honey bees

Summary Honey bee mating cannot be directly controlled in the same way as in many agriculturally important animals. Instrumental insemination is, however, possible and can be used as an aid in selective breeding. Hygienic behaviour, in which worker bees detect and remove dead or diseased brood from capped cells, is a heritable trait that confers colony-level resistance against brood diseases. Using the freeze-killed brood (FKB) bioassay we compared the levels of hygiene in colonies headed by daughter queens reared from hygienic mother colonies that were either instrumentally inseminated with sperm from drones reared from hygienic colonies or allowed to mate naturally with naturally-occurring drones. Hygiene levels were significantly higher in the colonies of the instrumentally inseminated queens than in the colonies of the naturally-mated queens. However, the hygiene levels in the naturally-mated colonies were encouragingly high and indicate that supplying beekeepers with naturally-mated queens, or virgin queens to mate locally, can result in colonies with high levels of hygiene.

Landscape Scale Study of the Net Effect of Proximity to a Neonicotinoid-Treated Crop on Bee Colony Health

Since 2013, the European Commission has restricted the use of three neonicotinoid insecticides as seed dressings on bee-attractive crops. Such crops represent an important source of forage for bees, which is often scarce in agro-ecosystems. However, this benefit has often been overlooked in the design of previous field studies, leaving the net impact of neonicotinoid treated crops on bees relatively unknown. Here, we determine the combined benefit (forage) and cost (insecticide) of oilseed rape grown from thiamethoxam-treated seeds on Bombus terrestris and Apis mellifera colonies. In April 2014, 36 colonies per species were located adjacent to three large oilseed rape fields (12 colonies per field). Another 36 were in three nearby locations in the same agro-ecosystem, but several kilometers distant from any oilseed rape fields. We found that Bombus colony growth and reproduction were unaffected by location (distant versus adjacent) following the two month flowering period. Apis colony and queen survival were unaffected. However, there was a small, but significant, negative relationship between honey and pollen neonicotinoid contamination and Apis colony weight gain. We hypothesize that any sublethal effects of neonicotinoid seed dressings on Bombus colonies are potentially offset by the additional foraging resources provided. A better understanding of the ecological and agronomic factors underlying neonicotinoid residues is needed to inform evidence-based policy.

Hygienic behaviour in Brazilian stingless bees

ABSTRACT Social insects have many defence mechanisms against pests and pathogens. One of these is hygienic behaviour, which has been studied in detail in the honey bee, Apis mellifera. Hygienic honey bee workers remove dead and diseased larvae and pupae from sealed brood cells, thereby reducing disease transfer within the colony. Stingless bees, Meliponini, also rear broods in sealed cells. We investigated hygienic behaviour in three species of Brazilian stingless bees (Melipona scutellaris, Scaptotrigona depilis, Tetragonisca angustula) in response to freeze-killed brood. All three species had high mean levels of freeze-killed brood removal after 48 h ∼99% in M. scutellaris, 80% in S. depilis and 62% in T. angustula (N=8 colonies per species; three trials per colony). These levels are greater than in unselected honey bee populations, ∼46%. In S. depilis there was also considerable intercolony variation, ranging from 27% to 100% removal after 2 days. Interestingly, in the S. depilis colony with the slowest removal of freeze-killed brood, 15% of the adult bees emerging from their cells had shrivelled wings indicating a disease or disorder, which is as yet unidentified. Although the gross symptoms resembled the effects of deformed wing virus in the honey bee, this virus was not detected in the samples. When brood comb from the diseased colony was introduced to the other S. depilis colonies, there was a significant negative correlation between freeze-killed brood removal and the emergence of deformed worker bees (P=0.001), and a positive correlation with the cleaning out of brood cells (P=0.0008). This shows that the more hygienic colonies were detecting and removing unhealthy brood prior to adult emergence. Our results indicate that hygienic behaviour may play an important role in colony health in stingless bees. The low levels of disease normally seen in stingless bees may be because they have effective mechanisms of disease management, not because they lack diseases. Summary: Hygienic behaviour such as the removal of dead and diseased larvae and pupae has an important role in colony health in stingless bees, and it is greater than in unselected honey bee populations

First record of small hive beetle, Aethina tumida Murray, in South America

We report the discovery of adult small hive beetles, Aethina tumida, in a honey bee, Apis mellifera, apiary in Piracicaba, São Paulo State, Brazil, in March 2015. This is the first record for South America of this honey bee pest.

Towards integrated control of varroa: 4) varroa mortality from treating broodless winter colonies twice with oxalic acid via sublimation

In winter 2014–2015, we treated 22 broodless honey bee colonies with 2.25 g oxalic acid (OA) via sublimation on 23 December 2014 and again on 6 January 2015. Varroa numbers were determined before and after OA application by extracting mites from samples of workers. Mean varroa mortality from both applications combined was 99.6%, which is greater than the 97.6% mortality from a single treatment shown by our previous research. We determined whether double OA application was more harmful than single application, by comparing 12 colonies that had been double treated with 12 single-treated colonies. There was no difference in colony performance on 5 May 2015 (100% survival in both groups; 5.5 frames of brood in single-treated colonies vs. 5.3 in double-treated colonies). Varroa mortality from the first application, 96.8%, was significantly higher, p < 0.001, than from the second 87.2%. Ten of the 22 study colonies were killed 14 days after the second OA application to precisely quantify varroa levels. The mean number surviving was 6 (range 2–18). Worker numbers averaged 5,644 bees (range 3,352–8,692). To confirm the results a small second trial was made the following winter with 10 colonies. Results were similar. Again, combined varroa mortality was very high, 99.4%, with greater mortality from the first, 98.3%, than the second, 64.1%, application. Overall, the results indicate that double application of OA is worthwhile to beekeepers in varroa management. It is not harmful to colonies and by killing c. 99.5% of the varroa it reduces varroa populations to such an extent that 7–8 doublings, which would take more than one year, are needed to build back to the original level.

Quality versus quantity: foraging decisions in the honeybee (Apis mellifera scutellata) feeding on wildflower nectar and fruit juice

Abstract Foraging animals must often decide among resources which vary in quality and quantity. Nectar is a resource that exists along a continuum of quality in terms of sugar concentration and is the primary energy source for bees. Alternative sugar sources exist, including fruit juice, which generally has lower energetic value than nectar. We observed many honeybees (Apis mellifera scutellata) foraging on juice from fallen guava (Psidium guajava) fruit near others foraging on nectar. To investigate whether fruit and nectar offered contrasting benefits of quality and quantity, we compared honeybee foraging performance on P. guajava fruit versus two wildflowers growing within 50 m, Richardia brasiliensis and Tridax procumbens. Bees gained weight significantly faster on fruit, 2.72 mg/min, than on either flower (0.17 and 0.12 mg/min, respectively). However, the crop sugar concentration of fruit foragers was significantly lower than for either flower (12.4% vs. 37.0% and 22.7%, respectively). Fruit foragers also spent the most time handling and the least time flying, suggesting that fruit juice was energetically inexpensive to collect. We interpret honeybee foraging decisions in the context of existing foraging models and consider how nest‐patch distance may be a key factor for central place foragers choosing between resources of contrasting quality and quantity. We also discuss how dilute solutions, such as fruit juice, can help maintain colony sugar–water balance. These results show the benefits of feeding on resources with contrasting quality and quantity and that even low‐quality resources have value.