Mite‐y bees: bumble bees (Bombus spp., Hymenoptera: Apidae) host a relatively homogeneous mite (Acari) community,shaped by bee species identity but not by geographic proximity

1. Parasites can affect the communities of their hosts; and hosts, in turn, shape communities of parasites and other symbionts. This makes host–symbiont relationships a key but often overlooked aspect of community ecology. 2. Mites associated with bees have a range of lifestyles; however, little is known about mites associated with wild bees or about factors influencing the make‐up of bee‐associated mite communities. This study investigated how mite communities associated with bumble bees (Bombus spp.) are shaped by the Bombus community and geographic proximity. 3. Bees were collected from 15 sites in Ontario, Canada, and examined for mites. Mite abundance and species richness increased with local bee abundance. Several bee species also differed in mite abundance, species richness, prevalence, and diversity. Locally uncommon species tended to have more mites than other bees. Queen bees had the most mites, and males had more mites than workers. 4. Spatial proximity was not a predictor of mite community composition, despite a strong effect of proximity on bee community similarity. 5. On the 11 Bombus spp. examined, 33 mite species were found. Whereas nearly half of these mite species are obligate associates of bumble bees, none was restricted to particular Bombus species. 6. The best predictor of mite community composition was bee identity. Although many parasite communities show strong geographic patterns, the communities of primarily commensalistic bee‐mites in this study did not. These findings have implications for bumble bee conservation, given that pollen‐feeding commensals might become harmful at high densities or act as disease vectors.     

Comparison of the fecundity of three species of grain store mites on fungal diets

The egg production of isolated pairs ofAcarus siro, Glycyphagus destructor andTyrophagus longior fed on a control diet of wheatgerm and yeast was compared with that on mycelial pellets from shake cultures ofCladosporium cladosporiodes, Aspergillus repens, A. ruber andPenicillium cyclopium as well as spores ofP. cyclopium andA. repens. The mites always produced fewer eggs on the fungal diets than on the ideal diet.Tyrophagus longior usually did best of the three mite species on the fungal diets, andG. destructor worst.Aspergillus ruber proved the most suitable fungus for all mite species, whileC. cladosporiodes was the least suitable. Spores were a less suitable diet than mycelial pellets from shake cultures, which were predominantly mycelium.     

Transfers ofVarroa mites from newly emerged bees: Preferences for age- and function-specific adult bees (Hymenoptera: Apidae)

Movements of the parasitic honey bee mite,Varroa jacobsoni (Oud.) were monitored in several assays as they moved among adult host honey bees,Apis mellifera. We examined the propensity of mites to leave their hosts and to move onto new bee hosts. We also examined their preference for bees of different age and hive function. Mites were standardized by selecting mites from newly emerged worker bees (NEWs). In closed jars, 50% ofVarroa left NEWs irreversibly when no physical path was present for the mites to return to the NEWs; about 90% of mites left newly emerged drones in identical assays. In petri dish arenas, mites were rarely seen off NEW hosts when monitored at 15-min intervals for 4 h; this was the case for single NEWs with one mite (NEWs+) and when a NEW+ and a NEW− (no mites) were placed together in a petri dish. When a NEW+ was held with either a nurse beeor a pollen forager, 25% of the mites moved to the older bees. When both a nurseand a pollen forager were placed in a petri dish with a NEW+, about 50% of the mites transferred to older bees; nurse bees received about 80% of these mites, whereas pollen foragers received significantly fewer mites (about 20%,P < 0.05). Most mite transfers occurred during the first 30 min after combining NEWs+ and test bees. When NEWs+ were combined with bees of known ages, rather than function, mites transferred more often to young bees than to older bees (1- and 5-day-old bees vs. 25-day-old bees,P < 0.05; 1-day-old vs. 13- and 25-day-old bees;P < 0.05). No differences in proportions of transferring mites were seen when the range of bee ages was ≤ 8 days (P > 0.05), implying that the factors mediating the mites’ adult-host preference change gradually with bee age. A possible chemical basis for host choice byVarroa is indicated by their greater propensity to move onto freezer-killed nurse bees than onto freezer-killed pollen foragers (P < 0.05) and by their lower movement onto heat-treated bees than onto control bees (P < 0.05). Bee age, hive function, and directional changes in cuticular chemistry are all correlated. Movements of newly emerged mites in relation to these variables may provide insights into their reproductive success inApis mellifera colonies.     

Influence of resistant honey bee hosts on the life history of the parasite Acarapis woodi

Non-infested, young adult honey bees (Apis mellifera L.) of two stocks were exposed to tracheal mites (Acarapis woodi (Rennie)) in infested colonies to determine how divergent levels of susceptibility in host bees differentially affect components of the mite life history. Test bees were retrieved after exposure and dissected to determine whether resistance is founded on the reduced success of gravid female (foundress) mites to enter the host tracheae, on the suppressed reproduction by foundress mites once established in host tracheae or on both. Cohorts of 30–60 bees from each of ten resistant colonies and eight susceptible colonies were tested in eight trials (three to five colonies per stock per trial) having exposure durations of 4, 9 or 21 days. The principal results were that lower percentages of resistant bees than of susceptible bees routinely became infested by foundress mites, individual infested susceptible bees often had more foundress mites than individual infested resistant bees did and mite fecundity was similar in both host types. The infestation percentage results corresponded well with similar results from a prior field test of these stocks and, thus, suggest that the bioassay is useful for assessing honey bee resistance to A. woodi.     

Development of a user-friendly delivery method for the fungus Metarhiziumanisopliae to control the ectoparasitic mite Varroa destructor in honey bee, Apis mellifera, colonies

A user-friendly method to deliver Metarhizium spores to honey bee colonies for control of Varroa mites was developed and tested. Patty blend formulations protected the fungal spores at brood nest temperatures and served as an improved delivery system of the fungus to bee hives. Field trials conducted in 2006 in Texas using freshly harvested spores indicated that patty blend formulations of 10 g of conidia per hive (applied twice) significantly reduced the numbers of mites per adult bee, mites in sealed brood cells, and residual mites at the end of the 47-day experimental period. Colony development in terms of adult bee populations and brood production also improved. Field trials conducted in 2007 in Florida using less virulent spores produced mixed results. Patty blends of 10 g of conidia per hive (applied twice) were less successful in significantly reducing the number of mites per adult bee. However, hive survivorship and colony strength were improved, and the numbers of residual mites were significantly reduced at the end of the 42-day experimental period. The overall results from 2003 to 2008 field trials indicated that it was critical to have fungal spores with good germination, pathogenicity and virulence. We determined that fungal spores (1 × 10¹⁰ viable spores per gram) with 98% germination and high pathogenicity (95% mite mortality at day 7) provided successful control of mite populations in established honey bee colonies at 10 g of conidia per hive (applied twice). Overall, microbial control of Varroa mite with M. anisopliae is feasible and could be a useful component of an integrated pest management program.     

Comparison of diagnostic methods for detection of low infestation levels ofVarroa jacobsoni in honey-bee (Apis mellifera) colonies

Thirty-five honey-bee colonies, originally free fromVarroa jacobsoni (Oudemans) were monitored approximately every third week for the presence of the mite during 16 months following an initial introduction of five to eight adultVarroa females in early July. Investigations of hive debris detected the presence ofV. jacobsoni in 22 colonies (63%) within three months of the mite introduction. During the first winter period (October–April), mites were found in the hive debris of 13 colonies (37%). In terms of detectingVarroa during the summer in colonies with sealed brood, investigations of hive debris were more effective than sampling of brood. Brood sampling was more effective than sampling of live bees. In colonies without sealed brood, investigations of hive debris or of live bee samples seemed approximately equally efficient. The highest correlation between sampling methods was found between daily mite downfall and mites per live bee (r=0.81) in colonies with sealed brood. During the winter, investigations of dead bees and hive debris were approximately equally efficient in detectingVarroa.     

Low parasite loads accompany the invading population of the bumblebee, Bombus terrestris in Tasmania

In its native Europe, the bumblebee, Bombus terrestris (L.) has co-evolved with a large array of parasites whose numbers are negatively linked to the genetic diversity of the colony. In Tasmania B. terrestris was first detected in 1992 and has since spread over much of the state. In order to understand the bee’s invasive success and as part of a wider study into the genetic diversity of bumblebees across Tasmania, we screened bees for co-invasions of ectoparasitic and endoparasitic mites, nematodes and micro-organisms, and searched their nests for brood parasites. The only bee parasite detected was the relatively benign acarid mite Kuzinia laevis (Dujardin) whose numbers per bee did not vary according to region. Nests supported no brood parasites, but did contain the pollen-feeding life stages of K. laevis. Upon summer-autumn collected drones and queens, mites were present on over 80% of bees, averaged ca. 350–400 per bee and were more abundant on younger bees. Nest searching spring queens had similar mite numbers to those collected in summer-autumn but mite numbers dropped significantly once spring queens began foraging for pollen. The average number of mites per queen bee was over 30 fold greater than that reported in Europe. Mite incidence and mite numbers were significantly lower on worker bees than drones or queens, being present on just 51% of bees and averaging 38 mites per bee. Our reported incidence of worker bee parasitism by this mite is 5–50 times higher than reported in Europe. That only one parasite species co-invaded Tasmania supports the notion that a small number of queens founded the Tasmanian population. However, it is clearly evident that both the bee in the absence of parasites, and the mite have been extraordinarily successful invaders. Received 12 April 2006; revised 10 November 2006; accepted 15 November 2006.     

Selection for barriers between honey bees and a devastating parasite

Rivaling pesticides and a dearth of flowers, the parasitic mite Varroa destructor presents a tremendous threat to western honey bees, Apis mellifera. A longstanding, but minor, pest for the Asian honey bee Apis cerana, these obligate bee parasites feast on developing and adult A. mellifera across several continents. Varroa reproduction is limited to a short window when developing bee pupae are concealed in wax cells. Mated females target developing bees just before pupation and then have about one day to initiate reproduction, eventually laying one male and up to several female offspring. Female mites often fail to reproduce at all, instead waiting in cells until their bee host finishes development and then hitching dangerous rides on a succession of adult bees for up to several weeks, before scouting for a new host pupa. In this issue of Molecular Ecology, Conlon et al. (2019) have explored mite reproductive success via a clever and thought‐provoking association study. In so doing, they have identified a protein whose actions could be integral to the dance between bees and their mite parasites.     

Oxalic acid: a prospective tool for reducing <Emphasis Type="Italic">Varroa</Emphasis> mite populations in package bees

Numerous studies have investigated using oxalic acid (OA) to control Varroa mites in honey bee colonies. In contrast, techniques for treating package bees with OA have not been investigated. The goal of this study was to develop a protocol for using OA to reduce mite infestation in package bees. We made 97 mini packages of Varroa-infested adult bees. Each package contained 1,613 ± 18 bees and 92 ± 3 mites, and represented an experimental unit. We prepared a 2.8% solution of OA by mixing 35 g OA with 1 l of sugar water (sugar:water = 1:1; w:w). Eight treatments were assigned to the packages based on previous laboratory bioassays that characterized the acute contact toxicity of OA to mites and bees. We administered the treatments by spraying the OA solution directly on the bees through the mesh screen cage using a pressurized air brush and quantified mite and bee mortality over a 10-day period. Our results support applying an optimum volume of 3.0 ml of a 2.8% OA solution per 1,000 bees to packages for effective mite control with minimal adult bee mortality. The outcome of our research provides beekeepers and package bee shippers guidance for using OA to reduce mite populations in package bees.     

The resistance mechanism of the Asian honey bee,Apis cerana Fabr., to an ectoparasitic mite,Varroa jacobsoni Oudemans

A behavioral and physiological resistance mechanism of the Asian honey bee (Apis cerana) to an ectoparasitic mite, Varroa jacobsoni, which causes severe damage to the European honey bee (Apis mellifera) in the beekeeping industry worldwide, is reported here for the first time. Parasitism by the mite induced Asian worker bees to perform a series of cleaning behaviors that effectively removed the mites from the bodies of the adult host bees. The mites were subsequently killed and removed from the bee hives in a few seconds to a few minutes. The grooming behavior consists of self-cleaning, grooming dance, nestmate cleaning, and group cleaning. Worker bees can also rapidly and effectively remove the mites from the brood. The European bee showed cleaning behavior at low frequency and generally failed to remove the mites from both the adult bees and the brood.     

Host-seeking behaviour of tracheal mites (Acari: Tarsonemidae) on honey bees (Hymenoptera: Apidae)

The behaviour of the endoparasitic tracheal mite, Acarapis woodi (Rennie) on honey bees (Apis mellifera L.) is a challenge to observe because of its small size. Through a microscope, we videotaped this mite's movement on young bees, dead bees and bees exposed to vegetable oil. Previous studies have shown that solid vegetable oil decreases mite infestations in a bee colony. We hypothesized that the oil alters mite behaviour to the detriment of the parasite, thus helping to safeguard the host. Habitat-seeking behaviour, identified as necessary for mites to locate a new host environment, was disrupted on both dead and oil-treated bees. Questing behaviour, which is associated with transfer between hosts, increased significantly on the dead and oily bees. The behaviours of mites were significantly different between all three treatments (x ²=494.96, p<0.001 on dead bees and x ²=851.11, p<0.001 on oily bees). Both questing and seeking behaviours were significantly different on each of the thoracic treatments (F _2,66=7.88, p<0.001 and F _2,66=21.28, p<0.001) and mite questing behaviour was not altered between males and females on live or oily bees (F _1,22=0.25, p<0.62), but habitat seeking was (F _1,22=7.42, p<0.012). The male questing and habitat-seeking behaviours were observed. We conclude that oil-treated bees gained protection from habitat-seeking mites because the normal behaviour of the mites seeking an oviposition site is interrupted.     

Some observations on the concurrent parasitization ofApis florea byTropilaelaps clareae andEuvarroa sinhai

Adult bees, worker brood cells and drone brood cells ofApis florea were examined for the presence of mites by stereo microscope and by washing with soap. Tropilaelaps clareae was only found on adult bees;Euvarroa sinhai on adult bees and drone brood. The level ofT. clareae infestation is always very low, generally not exceeding 0.1%; that ofE. sinhai is somewhat higher. The mites were never found together on a single bee.     

Host preference of the honey bee tracheal mite (Acarapis woodi (Rennie))

Field and laboratory bioassays were used to test the preference of the honey bee tracheal mite,Acarapis woodi (Rennie), for drones versus workers. Groups of newly-emerged drones and workers were marked and introduced into either heavily infested colonies (field bioassays) or into the cages of infested bees obtained from the field colonies (laboratory bioassays). Seven days later all of the marked bees in each bioassay were removed. The numbers of mites of each life stage in each drone or worker target bee of each experiment were quantified. Mite prevalence values for the two castes were not found to differ significantly for either experiment. However, the caste of the target bee was shown to influence the migration of the adult female mites. Drones contained a greater number of migratory female mites and greater total numbers of all mite stages as compared to workers. These results indicate that migrating female mites preferentially infest drones and suggest that the role of drones in the dissemination and population dynamics of the tracheal mite needs to be examined further.     

The effects of temperature and dose of formic acid on treatment efficacy against Varroa destructor (Acari: Varroidae), a parasite of Apis mellifera (Hymenoptera: Apidae)

In order to decrease the variability of formic acid treatments against the honey bee parasite the varroa mite, Varroa destructor, it is necessary to determine the dose-time combination that best controls mites without harming bees. The concentration × time (CT) product is a valuable tool for studying fumigants and how they might perform under various environmental conditions. This laboratory study is an assessment of the efficacy of formic acid against the varroa mite under a range of formic acid concentrations and temperatures. The objectives are 1) to determine the effect of temperature and dose of formic acid on worker honey bee and varroa mite survival, 2) to determine the CT₅₀ products for both honey bees and varroa mites and 3) to determine the best temperature and dose to optimize selectivity of formic acid treatment for control of varroa mites. Worker honey bees and varroa mites were fumigated at 0, 0.01, 0.02, 0.04, 0.08, and 0.16 mg/L at 5, 15, 25, and 35 °C for 12 d. Mite and bee mortality were assessed at regular intervals. Both mite and bee survival were affected by formic acid dose. Doses of 0.08 and 0.16 mg/L were effective at killing mites at all temperatures tested above 5 °C. There was a significant interaction between temperature, dose, and species for the CT₅₀ product. The difference between the CT₅₀ product of bees and mites was significant at only a few temperature-dose combinations. CT product values showed that at most temperatures the greatest fumigation efficiency occurred at lower doses of formic acid. However, the best fumigation efficiency and selectivity combination for treatments occurred at a dose of 0.16 mg/L when the temperature was 35 °C. This revised version was published online in July 2006 with corrections to the Cover Date.     

Deformed wing virus associated with <Emphasis Type="Italic">Tropilaelaps mercedesae</Emphasis> infesting European honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Mites in the genus Tropilaelaps (Acari: Laelapidae) are ectoparasites of the brood of honey bees (Apis spp.). Different Tropilaelaps subspecies were originally described from Apis dorsata, but a host switch occurred to the Western honey bee, Apis mellifera, for which infestations can rapidly lead to colony death. Tropilaelaps is hence considered more dangerous to A. mellifera than the parasitic mite Varroa destructor. Honey bees are also infected by many different viruses, some of them associated with and vectored by V. destructor. In recent years, deformed wing virus (DWV) has become the most prevalent virus infection in honey bees associated with V. destructor. DWV is distributed world-wide, and found wherever the Varroa mite is found, although low levels of the virus can also be found in Varroa free colonies. The Varroa mite transmits viral particles when feeding on the haemolymph of pupae or adult bees. Both the Tropilaelaps mite and the Varroa mite feed on honey bee brood, but no observations of DWV in Tropilaelaps have so far been reported. In this study, quantitative real-time RT-PCR was used to show the presence of DWV in infested brood and Tropilaelaps mercedesae mites collected in China, and to demonstrate a close quantitative association between mite-infested pupae of A. mellifera and DWV infections. Phylogenetic analysis of the DWV sequences recovered from matching pupae and mites revealed considerable DWV sequence heterogeneity and polymorphism. These polymorphisms appeared to be associated with the individual brood cell, rather than with a particular host.     

Efficacy of strips coated with Metarhizium anisopliae for control of Varroa destructor (Acari: Varroidae) in honey bee colonies in Texas and Florida

Strips coated with conidia of Metarhizium anisopliae (Metschinkoff; Deuteromycetes: Hyphomycetes) to control the parasitic mite, Varroa destructor (Anderson and Trueman) in colonies of honey bees, Apis mellifera (Hymenoptera: Apidae) were compared against the miticide, tau-fluvalinate (Apistan) in field trials in Texas and Florida (USA). Apistan and the fungal treatments resulted in successful control of mite populations in both locations. At the end of the 42-day period of the experiment in Texas, the number of mites per bee was reduced by 69-fold in bee hives treated with Apistan and 25-fold in hives treated with the fungus; however mite infestations increased by 1.3-fold in the control bee hives. Similarly, the number of mites in sealed brood was 13-fold and 3.6-fold higher in the control bee hives than in those treated with Apistan and with the fungus, respectively. Like the miticide Apistan, the fungal treatments provided a significant reduction of mite populations at the end of the experimental period. The data from the broodless colonies treated with the fungus indicated that optimum mite control could be achieved when no brood is being produced, or when brood production is low, such as in the early spring or late fall. In established colonies in Florida, honey bee colony development did not increase under either Apistan or fungal treatments at the end of the experimental period, suggesting that other factors (queen health, food source, food availability) play some major role in the growth of bee colonies. Overall, microbial control of Varroa mites with fungal pathogens could be a useful component of an integrated pest management program for the honey bee industry.     

The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels

Wet weight, dry weight and water contents of emerging honeybees (Apis mellifera L. [Hymenoptera: Apidae]) infested with the ectoparasitic mite Varroa destructor (Anderson) (Acari: Varroidae) were all negatively correlated with increasing numbers of mites. It was estimated that for every female mite present during the bees' development, the host would lose three percent of its body water. Parasitised bees also emerged with lower head and abdomen concentrations of protein and with lower abdominal carbohydrate concentrations. Lipid concentrations were not detectably affected by V. destructor infestation. The losses of metabolic reserves were not, however, judged to be serious enough to be directly responsible for the high bee mortality and ultimate colony collapse that are associated with the arrival of Varroa in a hive. Some 8.5% of the emerging bees exhibited morphological deformities and deformity was positively correlated with increasing numbers of mites in brood cells. Deformed bees were, however, found in all categories of parasitosis, suggesting that other factors, such as infectious agents, may be involved. Mites that fed on either live or dead U¹⁴C- labelled bees acquired the label within 24 h and it was calculated that an adult female mite consumes 0.67 l haemolymph 24 h^–1. It was also demonstrated that ¹⁴C was transmitted to a previously non-radio-labelled bee when a mite that had been feeding on a labelled bee changed hosts. The level of transfer was above that which could have arisen through contamination of the mites' mouthparts and supports the suggestion that Varroa is an important vector of pathogens such as viruses.     

Field trials using the fungal pathogen, Metarhizium anisopliae (Deuteromycetes: Hyphomycetes) to control the ectoparasitic mite, Varroa destructor (Acari: Varroidae) in honey bee, Apis mellifera (Hymenoptera: Apidae) colonies

The potential for Metarhizium anisopliae (Metschinkoff) to control the parasitic mite, Varroa destructor (Anderson and Trueman) in honey bee colonies was evaluated in field trials against the miticide, tau-fluvalinate (Apistan). Peak mortality of V. destructor occurred 3-4 d after the conidia were applied; however, the mites were still infected 42 d posttreatments. Two application methods were tested: dusts and strips coated with the fungal conidia, and both methods resulted in successful control of mite populations. The fungal treatments were as effective as the Apistan, at the end of the 42-d period of the experiment. The data suggested that optimum mite control could be achieved when no brood is being produced, or when brood production is low, such as in the early spring or late fall. M. anisopliae was harmless to the honey bees (adult bees, or brood) and colony development was not affected. Mite mortality was highly correlated with mycosis in dead mites collected from sticky traps, indicating that the fungus was infecting and killing the mites. Because workers and drones drift between hives, the adult bees were able to spread the fungus between honey bee colonies in the apiary, a situation that could be beneficial to beekeepers.     

Population growth of Varroa destructor (Acari: Varroidae) in commercial honey bee colonies treated with beta plant acids

Varroa (Varroa destuctor Anderson and Trueman) populations in honey bee (Apis mellifera L.) colonies might be kept at low levels by well-timed miticide applications. HopGuard^® (HG) that contains beta plant acids as the active ingredient was used to reduce mite populations. Schedules for applications of the miticide that could maintain low mite levels were tested in hives started from either package bees or splits of larger colonies. The schedules were developed based on defined parameters for efficacy of the miticide and predictions of varroa population growth generated from a mathematical model of honey bee colony–varroa population dynamics. Colonies started from package bees and treated with HG in the package only or with subsequent HG treatments in the summer had 1.2–2.1 mites per 100 bees in August. Untreated controls averaged significantly more mites than treated colonies (3.3 mites per 100 bees). By October, mite populations ranged from 6.3 to 15.0 mites per 100 bees with the lowest mite numbers in colonies treated with HG in August. HG applications in colonies started from splits in April reduced mite populations to 0.12 mites per 100 bees. In September, the treated colonies had significantly fewer mites than the untreated controls. Subsequent HG applications in September that lasted for 3 weeks reduced mite populations to levels in November that were significantly lower than in colonies that were untreated or had an HG treatment that lasted for 1 week. The model accurately predicted colony population growth and varroa levels until the fall when varroa populations measured in colonies established from package bees or splits were much greater than predicted. Possible explanations for the differences between actual and predicted mite populations are discussed.     

The Role of Cuticular Compounds in the Resistance of Honey Bees (Apis Mellifera) to Tracheal Mites (Acarapis Woodi)

This study examined the migration of tracheal mites (Acarapis woodi) into honey bees (Apis mellifera) from different colonies and the relative attraction of mites to hexane extracts from the external body surfaces of young bees. Relative resistance of bees from different colonies initially was assessed with a field bioassay that involved tagging newly emerged bees, pooling them in heavily mite-infested colonies, retrieving them 7 days later, and examining them for tracheal mite prevalence and abundance. For those colonies identified as most resistant and least resistant, cuticular chemicals were extracted in hexane from frozen, newly emerged worker bees. These extracts were presented to individual tracheal mites in pairwise fashion in a laboratory bioassay. The results demonstrated that mites prefer extracts of bees from some colonies more than others, however, no consistent differences were demonstrated. Our inability to predict mite responses to extracts based on our initial assessment of relative resistance indicates that other mechanisms of resistance influence mite success in colonizing new host bees.