Seasonal variation in the activity of selected antioxidant enzymes and malondialdehyde level in worker honey bees

The recent decline in managed honey bee populations, Apis mellifera L. (Hymenoptera: Apidae), has caused scientific, ecological, and economic concern. Research into the formation of reactive oxygen species (ROS), antioxidative defense mechanisms, and oxidative stress can contribute to our understanding of bee survival and conservation of this species. Activities of superoxide dismutase (SOD), catalase (CAT), and glutathione S‐transferase (GST) enzymes together with levels of malondialdehyde (MDA) were measured in summer and winter honey bees sampled from three colonies. One colony was stationary (C1), entering the winter period having accumulated Robinia pseudoacacia L. (Fabaceae) honey, and two were migratory (C2 and C3), entering the winter period with mainly Tilia (Malvaceae) and Brassica (Brassicaceae) honey, respectively. Compared to summer workers, winter worker bees had decreased SOD and GST activity, and MDA level, whereas CAT activity increased in all three colonies. We also demonstrated that seasonality is the main factor responsible for changes in antioxidant enzymes and MDA levels in worker honey bees. Overall, our results indicate a difference between summer and winter worker bees, pointing at a reduced level of antioxidant enzyme defenses during overwintering which may be due to a decrease in production of ROS. The decreased levels of MDA measured in winter honey bees confirm this. As ROS are actively used by insects as a defense mechanism to fight pathogens, we suggest that reduced production of ROS contributes to higher susceptibility of winter honey bees to infections and reduced overwinter survival.     

Causal Assessment of Biological Impairment in the Little Floyd River,Iowa, USA

An assessment of biological impairment in the Little Floyd River (Iowa, USA) was based on evidence of three characteristics of causation: co-occurrence, preceding causation, and sufficiency. Evidence of the physical interaction of the probable causes and the biota, resulting alterations to the biota, as well as the time order of the cause and the effect were consistent within the assessment, but the evidence for these causal characteristics did not discriminate among probable causes or other causes. Deposited sediment, low dissolved oxygen, heat stress, and ammonia toxicity are the probable causes of impaired biological condition in the Little Floyd River compared with other rivers in the ecoregion. Less likely causes are suspended sediment, altered basal food resources, and flow alteration. Very unlikely causes are pH shifts, total dissolved solids, Cyprinus carpio (an invasive species), metal toxicity, and pesticides. Data were insufficient to assess salinity or other toxicants. The assessment was used to develop a recovery plan for the stream. This assessment demonstrates that, even when there are many candidate causes and uncertainties are substantial, the probable causes of biological impairments can be determined with enough certainty to inform decision-making to address environmental problems.     

Thinking beyond Western commercial honeybee hives: towards improved conservation of honey bee diversity

A decline of wild pollinators, along with a decline of bee diversity, has been a cause of concern among academics and governmental organizations. According to IPBES, a lack of wild pollinator data contributes to difficulties in comprehensively analyzing the regional status of wild pollinators in Africa, Latin America, Asia and Oceania. It may have also contributed to the prevailing lack of awareness of the diversity of honey bees, of which the managed Apis mellifera is often considered as “the (only) honey bee,” despite the fact that there are eight other honey bee species extant in Asia. A survey of 100 journal articles published in 2016 shows that 57% of the studies still identified A. mellifera as “the honey bee.” In total, 80% of studies were conducted solely on A. mellifera. This focus on A. mellifera has also caused the honey standard of Codex Alimentarius and the European Union to be based solely on A. mellifera, causing improper evaluation of honeys from other species. We recommend adapting current standards to reflect the diversity of honey bees and in the process correct failures in the honey market and pave the way towards improved protection of honey bee species and their habitats.     

A push‐pull integrated pest management scheme for preventing use of parrot nest boxes by invasive Africanized honey bees

Africanized honey bees (Apis mellifera scutellata) compete with endangered parrots for nest boxes and can hamper conservation efforts. We tested an integrated pest management push‐pull protocol in the Atlantic Forest in São Paulo, Brazil, in an effort to prevent bee swarms from colonizing nest boxes (N = 30 in the forest plus five in aviaries) meant for use by Vinaceous‐breasted Amazons (Amazona vinacea). Fifteen parrot nest boxes were treated with a permethrin insecticide to “push” scout bees away and each parrot box was paired with a bee trap box containing a pheromone lure to “pull” bees. Over a 1‐yr period (March 2013 to March 2014), 29 insect colonies moved into 18 of the 35 trap boxes. Nine Africanized honey bee, three native Jatai bee (Tetragonisca sp.), and 17 wasp colonies occupied trap boxes. Only one experimental push‐pull pair untreated parrot box was invaded by bees and no parrot boxes in aviaries were colonized. Four of the parrot nest boxes were occupied by birds during our study. Although none were used by Vinaceous‐breasted Amazons, Southern House Wrens (Troglodytes musculus), Green‐winged Saltators (Saltator similis), and Plain Parakeets (Brotogeris tirica) nested in the boxes and all nests were successful. Although long‐term studies are needed before drawing conclusions about the effectiveness of trap boxes, our results suggest that a push‐pull protocol may prove useful for reducing the use of nest boxes meant for parrots and other cavity‐nesting birds by Africanized honey bees and other insects.     

Orchard pollination in Capitol Reef National Park,Utah, USA. Honey bees or native bees?

Capitol Reef National Park in central Utah, USA surrounds 22 managed fruit orchards started over a century ago by Mormon pioneers. Honey bees are imported for pollination, although the area in which the Park is embedded has over 700 species of native bees, many of which are potential orchard pollinators. We studied the visitation of native bees to apple, pear, apricot, and sweet cherry over 2 years. Thirty species of bees visited the flowers but, except for pear flowers, most were uncommon compared to honey bees. Evidence that honey bees prevented native bees from foraging on orchard crop flowers was equivocal: generally, honey bee and native bee visitation rates to the flowers were not negatively correlated, nor were native bee visitation rates positively correlated with distance of orchards from honey bee hives. Conversely, competition was tentatively suggested by much larger numbers of honey bees than natives on the flowers of apples, apricots and cherry; and by the large increase of native bees on pears, where honey bee numbers were low. At least one-third of the native bee species visiting the flowers are potential pollinators, including cavity-nesting species such as Osmia lignaria propinqua, currently managed for small orchard pollination in the US, plus several fossorial species, including one rosaceous flower specialist (Andrena milwaukiensis). We suggest that gradual withdrawal of honey bees from the Park would help conserve native bee populations without decreasing orchard crop productivity, and would serve as a demonstration of the commercial value of native pollinators.     

Exposure of the wild bee Osmia bicornis to the honey bee pathogen Nosema ceranae

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Russian honey bee (Hymenoptera: Apidae) colonies: Acarapis woodi (Acari: Tarsonemidae) infestations and overwintering survival

Honey bee, Apis mellifera L. (Hymenoptera: Apidae), colonies infested by parasitic mites are more prone to suffer from a variety of stresses, including cold temperature. We evaluated the overwintering ability of candidate breeder lines of Russian honey bees, most of which are resistant to both Varroa destructor Anderson & Trueman and Acarapis woodi (Rennie), during 1999-2001. Our results indicate that Russian honey bee colonies (headed by original and supersedure queens) can successfully overwinter in the north, even during adverse weather conditions, owing to their frugal use of food stores and their resistance to tracheal mite infestations. In contrast, colonies of Italian honey bees consumed more food, had more mites, and lost more adult bees than Russian honey bees, even during unusually mild winter conditions.     

Winter survival of individual honey bees and honey bee colonies depends on level of Varroa destructor infestation

Background

Recent elevated winter loss of honey bee colonies is a major concern. The presence of the mite Varroa destructor in colonies places an important pressure on bee health. V. destructor shortens the lifespan of individual bees, while long lifespan during winter is a primary requirement to survive until the next spring. We investigated in two subsequent years the effects of different levels of V. destructor infestation during the transition from short-lived summer bees to long-lived winter bees on the lifespan of individual bees and the survival of bee colonies during winter. Colonies treated earlier in the season to reduce V. destructor infestation during the development of winter bees were expected to have longer bee lifespan and higher colony survival after winter.

Methodology/Principal Findings

Mite infestation was reduced using acaricide treatments during different months (July, August, September, or not treated). We found that the number of capped brood cells decreased drastically between August and November, while at the same time, the lifespan of the bees (marked cohorts) increased indicating the transition to winter bees. Low V. destructor infestation levels before and during the transition to winter bees resulted in an increase in lifespan of bees and higher colony survival compared to colonies that were not treated and that had higher infestation levels. A variety of stress-related factors could have contributed to the variation in longevity and winter survival that we found between years.

Conclusions/Significance

This study contributes to theory about the multiple causes for the recent elevated colony losses in honey bees. Our study shows the correlation between long lifespan of winter bees and colony loss in spring. Moreover, we show that colonies treated earlier in the season had reduced V. destructor infestation during the development of winter bees resulting in longer bee lifespan and higher colony survival after winter.     

Viral transmission in honey bees and native bees,supported by a global black queen cell virus phylogeny

In recent decades, we have realized that honey bee viruses are not, in fact, exclusive to honey bees. The potential impact of Apis-affiliated viruses on native pollinators is prompting concern. Our research addresses the issue of virus crossover between honey bees and native bees foraging in the same localities. We measured the presence of black queen cell virus (BQCV), deformed wing virus (DWV) and sacbrood virus (SBV) in managed Apis mellifera (honey bees) and native Andrena spp. (subgenus Melandrena) bee populations in five commercial orchards. We identified viral presence across sites and bees and related these data to measures of bee community diversity. All viruses were found in both managed and native bees, and BQCV was the most common virus in each. To establish evidence for viral crossover between taxa, we undertook an additional examination of BQCV where 74 samples were sequenced and placed in a global phylogenic framework of hundreds of BQCV strains. We demonstrate pathogen sharing across managed honey bees and distantly related wild bees. This phylogenetic analysis contributes to growing evidence for host switching and places local incidence patterns in a worldwide context, revealing multispecies viral transmission.     

Cover Caption

The Western honey bee, Apis mellifera (L.), is perhaps the most beneficial insect we know, mainly because of the pollination services it provides to fruits and vegetables. Honey bee workers show changes in behaviors as they age. Young bees typically are “nurses” and perform in‐hive tasks such as feeding larvae and take care of the queen, old bees become foragers and bring in food sources (nectar, pollen, and water) or propolis. Methoprene has been known to accelerate worker development so bees become foragers earlier, but its mechanisms were not known. In this study Huang et al. show that most likely methoprene works directly on hormone receptors to mimic juvenile hormone, in causing bees to forage early (pages 235–240). Photo by Zachary Y. Huang. [Correction added on 17 April 2018, after first online publication: Cover caption has been revised.]     

Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection

Parasites are dependent on their hosts for energy to reproduce and can exert a significant nutritional stress on them. Energetic demand placed on the host is especially high in cases where the parasite-host complex is less co-evolved. The higher virulence of the newly discovered honeybee pathogen, Nosema ceranae, which causes a higher mortality in its new host Apis mellifera, might be based on a similar mechanism. Using Proboscis Extension Response and feeding experiments, we show that bees infected with N. ceranae have a higher hunger level that leads to a lower survival. Significantly, we also demonstrate that the survival of infected bees fed ad libitum is not different from that of uninfected bees. These results demonstrate that energetic stress is the probable cause of the shortened life span observed in infected bees. We argue that energetic stress can lead to the precocious and risky foraging observed in Nosema infected bees and discuss its relevance to colony collapse syndrome. The significance of energetic stress as a general mechanism by which infectious diseases influence host behavior and physiology is discussed.     

Parasite Pressures on Feral Honey Bees (Apis mellifera sp.)

Feral honey bee populations have been reported to be in decline due to the spread of Varroa destructor, an ectoparasitic mite that when left uncontrolled leads to virus build-up and colony death. While pests and diseases are known causes of large-scale managed honey bee colony losses, no studies to date have considered the wider pathogen burden in feral colonies, primarily due to the difficulty in locating and sampling colonies, which often nest in inaccessible locations such as church spires and tree tops. In addition, little is known about the provenance of feral colonies and whether they represent a reservoir of Varroa tolerant material that could be used in apiculture. Samples of forager bees were collected from paired feral and managed honey bee colonies and screened for the presence of ten honey bee pathogens and pests using qPCR. Prevalence and quantity was similar between the two groups for the majority of pathogens, however feral honey bees contained a significantly higher level of deformed wing virus than managed honey bee colonies. An assessment of the honey bee race was completed for each colony using three measures of wing venation. There were no apparent differences in wing morphometry between feral and managed colonies, suggesting feral colonies could simply be escapees from the managed population. Interestingly, managed honey bee colonies not treated for Varroa showed similar, potentially lethal levels of deformed wing virus to that of feral colonies. The potential for such findings to explain the large fall in the feral population and the wider context of the importance of feral colonies as potential pathogen reservoirs is discussed.     

Wild bee diversity is enhanced by experimental removal of timber harvest residue within intensively managed conifer forest

The use of timber harvest residue as an energy source is thought to have environmental benefits relative to food‐based crops, yet the ecological impact of this practice remains largely unknown. We assessed whether the abundance and diversity of wild bees (Apoidea) were influenced by the removal of harvest residue and associated soil compaction within managed conifer forest in western Oregon, USA. We sampled bees over two years (2014–2015) on study plots that were subjected to five treatments representing gradients in removal of harvest residue and soil compaction. We collected >7,500 bee specimens from 92 distinct species/morphospecies that represented five of the seven bee families. We trapped 3x more individuals in the second year of the study despite identical sampling effort in both years, with most trapped bees classified as ground‐nesting species. Members of the sweat bee family (Halictidae) comprised more than half of all specimens, and the most abundant genus was composed of metallic green bees (Agapostemon, 33.6%), followed by long‐horned bees (Melissodes, 16.5%), sweat bees (Halictus, 15.9%), and bumble bees (Bombus, 13.6%). In both years, abundance and observed species richness were greatest in the most intensive harvest residue treatment, with other treatments having similar values for both measures. Our study indicates that early successional managed conifer forest that has experienced removal of harvest residue can harbor a surprising diversity of wild bees, which are likely to have important contributions to the broader ecological community through the pollination services they provide.     

Identifying the sister group to the bees: a molecular phylogeny of Aculeata with an emphasis on the superfamily Apoidea

Debevec, AH., Cardinal, S & Danforth, BN. Identifying the sister group to the bees: a molecular phylogeny of Aculeata with an emphasis on the superfamily Apoidea. —Zoologica Scripta, 41, 527–535. The hymenopteran superfamily Apoidea includes the bees (Anthophila) as well as four predatory wasp families (Heterogynaidae, Ampulicidae, Sphecidae and Crabronidae) collectively referred to as the “sphecoid” or “apoid” wasps. The most widely cited studies suggest that bees are sister to the wasp family Crabronidae, but alternative hypotheses have been proposed based on both morphological and molecular data. We combined DNA sequence data from previously published studies and newly generated data for four nuclear genes (28S, long‐wavelength rhodopsin, elongation factor‐1α and wingless) to identify the likely sister group to the bees. Analysis of our four‐gene data set by maximum likelihood and Bayesian methods indicates that bees most likely arise from within a paraphyletic Crabronidae. Possible sister groups to the bees include Philanthinae, Pemphredoninae or Philanthinae + Pemphredoninae. We used Bayesian methods to explore the robustness of our results. Bayes Factor tests strongly rejected the hypotheses of crabronid monophyly as well as placement of Heterogynaidae within Crabronidae. Our results were also stable to alternative rootings of the bees. These findings provide additional support for the hypothesis that bees arise from within Crabronidae, rather than being sister to Crabronidae, thus altering our understanding of bee ancestry and evolutionary history.     

Venom replenishment,as indicated by histamine,in honey bee (Apis mellifera) venom

Venom resynthesis, as indicated by histamine, has been investigated in the venom system of worker honey bees.After depletion of the venom contained in the venom reservoir, by electrical “milking”, histamine resynthesis was most active between 18 and 24 hr after “milking”.The ability of a bee to resynthesise histamine is age dependent. Young bees show some resynthetic ability, two week old bees show maximal ability to replace histamine. This capability is gradually lost as bees age and is virtually absent in 40 day old bees.     

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.     

Deceptive orchids with Meliponini as pollinators

Visitation of orchids by Meliponini (stingless bees) is confirmed only in 13Melipona, Partamona andTrigona, forXylobium andMaxillaria, with the addition ofTrigona fulviventris visitingIonopsis. Some bees evinced multiple floral visitation by carrying several stipes and viscidia from pollinaria, thus may cause seed set. None foraged pseudopollen, nor is collection of this substance by bees verified. Meliponine-visited orchids had pollinia in quartets with emplacement on the bee's scutellum, possibly devices for pollinia survival on a social bee passing through its nest. Further, orchids produced no nectar, but bees repeatedly came to flowers. A testable basis for the orchid-meliponine relationship is mimicry of rewarding resources, or bee pheromone mimicry, recently documented for some honey bees. Meliponine pheromone analogs (nerol and 2-heptanol) are here noted forMaxillaria, but lack of foraging with pheromones byMelipona suggests multiple avenues of mimicry by orchids, including alarm pheromone and carrion mimicry.     

Urbanization Increases Pathogen Pressure on Feral and Managed Honey Bees

Given the role of infectious disease in global pollinator decline, there is a need to understand factors that shape pathogen susceptibility and transmission in bees. Here we ask how urbanization affects the immune response and pathogen load of feral and managed colonies of honey bees (Apis mellifera Linnaeus), the predominant economically important pollinator worldwide. Using quantitative real-time PCR, we measured expression of 4 immune genes and relative abundance of 10 honey bee pathogens. We also measured worker survival in a laboratory bioassay. We found that pathogen pressure on honey bees increased with urbanization and management, and the probability of worker survival declined 3-fold along our urbanization gradient. The effect of management on pathogens appears to be mediated by immunity, with feral bees expressing immune genes at nearly twice the levels of managed bees following an immune challenge. The effect of urbanization, however, was not linked with immunity; instead, urbanization may favor viability and transmission of some disease agents. Feral colonies, with lower disease burdens and stronger immune responses, may illuminate ways to improve honey bee management. The previously unexamined effects of urbanization on honey-bee disease are concerning, suggesting that urban areas may favor problematic diseases of pollinators.     

Bee- to bird-pollination shifts in <Emphasis Type="Italic">Penstemon</Emphasis>: effects of floral-lip removal and corolla constriction on the preferences of free-foraging bumble bees

Plants might be under selection for both attracting efficient pollinators and deterring wasteful visitors. Particular floral traits can act as exploitation barriers by discouraging the unwelcome visitors. In the genus Penstemon, evolutionary shifts from insect pollination to more efficient hummingbird pollination have occurred repeatedly, resulting in the convergent evolution of floral traits commonly present in hummingbird-pollinated flowers. Two of these traits, a reduced or reflexed lower petal lip and a narrow corolla, were found in a previous flight-cage study to affect floral handling time by bumble bees, therefore potentially acting as “anti-bee” traits affecting preference. To test whether these traits do reduce bumble bee visitation in natural populations, we manipulated these two traits in flowers of bee-pollinated Penstemon strictus to resemble hummingbird-adapted close relatives and measured the preferences of free-foraging bees. Constricted corollas strongly deterred bee visitation in general, and particularly reduced visits by small bumble bees, resulting in immediate specialization to larger, longer-tongued bumble bees. Bees were also deterred—albeit less strongly—by lipless flowers. However, we found no evidence that lip removal and corolla constriction interact to further affect bee preference. We conclude that narrow corolla tubes and reduced lips in hummingbird-pollinated penstemons function as exploitation barriers that reduce bee access to nectaries or increase handling time.     

Honey bee (Hymenoptera: Apidae) distribution and potential for supplementary pollination in commercial tomato greenhouses during winter

This study examined the use of honey bees, Apis mellifera L., to supplement bumble bee, Bombus spp., pollination in commercial tomato, Lycopersicon esculentum Miller, greenhouses in Western Canada. Honey bee colonies were brought into greenhouses already containing bumble bees and left for 1 wk to acclimatize. The following week, counts of honey and bumble bees foraging and flying throughout the greenhouse were conducted three times per day, and tomato flowers open during honey bee pollination were marked for later fruit harvest. The same counts and flower-marking also were done before and after the presence of honey bees to determine the background level of bumble bee pollination. Overall, tomato size was not affected by the addition of honey bees, but in one greenhouse significantly larger tomatoes were produced with honey bees present compared with bumble bees alone. In that greenhouse, honey bee foraging was greater than in the other greenhouses. Honey bees generally foraged within 100 m of their colony in all greenhouses. Our study invites further research to examine the use of honey bees with reduced levels of bumble bees, or as sole pollinators of greenhouse tomatoes. We also make specific recommendations for how honey bees can best be managed in greenhouses.