Behavioral responses of the small hive beetle,Aethina tumida,to odors of three meliponine bee species and honey bees,Apis mellifera scutellata

Recent studies have shown that honey bees, bumble bees, and some meliponine bee species of the genera Trigona, Meliponula, and Dactylurina are hosts of the small hive beetle (SHB) Aethina tumidaMurray (Coleoptera: Nitidulidae), a pest of honey bee colonies in various regions of the world. Olfaction has been implicated in SHB infestations of honey bee and bumble bee colonies. We used olfactometer bioassays to investigate responses of adult male and female SHBs to odors from intact colonies and separate hive components (pot honey, pot pollen, cerumen, and propolis) of three African meliponine bee species, Meliponula ferruginea (Lepeletier) (black morphospecies), M. ferruginea (reddish brown morphospecies), and Meliponula bocandei (Spinola) (Hymenoptera: Apidae). Although both sexes of the beetle strongly preferred intact colony, pot honey, and pot pollen odors, there was no evidence of attraction to propolis and cerumen odors from the three meliponine bee species. Both sexes of SHB also strongly preferred odors from honey bees, Apis mellifera L. (Hymenoptera: Apidae), over odors from the three meliponine bee species. Our results provide substantial evidence of the host potential of African meliponine bees for the SHB, and we discuss this complex association of the SHB with species within the Apidae family.     

Temperature-Dependent Clustering Behavior of Aethina Tumida Murray in Apis Mellifera L. Colonies

Temperate races of honey bees (Apis mellifera) are able to survive cold temperatures by forming thermoregulatory clusters. Small hive beetles (Aethina tumida), which inhabit honey bee colonies in their native range of sub-Saharan Africa and in their introduced ranges of the United States and Australia, are able to endure temperate climates by entering the bee cluster when cold temperatures persist. We conducted an experiment to address the temporal aspects of the cluster-entering behavior of small hive beetles. We did this by exposing beetle-infested observation bee hives to different ambient temperatures and counting the number of beetles remaining in confinement sites on the hive’s periphery at each temperature. The resulting regression analyses suggest that the beetles enter the cluster more rapidly than they exit it, a behavior possibly linked to a colony’s decision to form and dismantle a cluster.     

Key factors influencing forager distribution across macadamia orchards differ among species of managed bees

To achieve maximised and sustainable crop productivity, it is critical that we develop crop-specific strategies for managing pollination. Honey bees (Apis mellifera) and stingless bees (Tetragonula carbonaria) are considered effective pollinators of macadamia (Macadamia integrifolia). The introduction of managed honey bee or stingless bee hives into orchards is likely to boost the numbers of these insects visiting flowers; however, there is a lack of published information and consensus regarding their management for pollination. Here, we identify factors that affect the distribution of both honey bees and stingless bees across cultivated macadamia, and establish whether increased flower visitation leads to higher nut set. A gradient of bee visitation rates was created by placing colonies on the ends of a four-hectare block, and mixed-effect models were applied to assess forager abundance and nut set with respect to distance from hive, time of day, cultivar, and floral display size. Distance from colony had a strong effect on stingless bee numbers, with >96% of individuals recorded within 100 metres of colonies, whereas the distribution of honey bees was more closely related to daily floral display: trees with greater numbers of flowers attracted more honey bees. Simplified surveys conducted in a further 17 macadamia blocks confirm that these are broadly occurring distribution patterns. Bee abundance alone did not significantly predict nut production; however, an indirect effect of bee visits to flowers is inferred, as nut production increased with size of floral display. To encourage a more even distribution of bees and uniform pollination, we recommend placement of stingless bee hives to maximise their distribution through a block (e.g. at 100-m intervals) and management practices that promote even distributions of flowers across trees.     

Unique Honey Bee (Apis mellifera) Hive Component-Based Communities as Detected by a Hybrid of Phospholipid Fatty-Acid and Fatty-Acid Methyl Ester Analyses

Microbial communities (microbiomes) are associated with almost all metazoans, including the honey bee Apis mellifera. Honey bees are social insects, maintaining complex hive systems composed of a variety of integral components including bees, comb, propolis, honey, and stored pollen. Given that the different components within hives can be physically separated and are nutritionally variable, we hypothesize that unique microbial communities may occur within the different microenvironments of honey bee colonies. To explore this hypothesis and to provide further insights into the microbiome of honey bees, we use a hybrid of fatty acid methyl ester (FAME) and phospholipid-derived fatty acid (PLFA) analysis to produce broad, lipid-based microbial community profiles of stored pollen, adults, pupae, honey, empty comb, and propolis for 11 honey bee hives. Averaging component lipid profiles by hive, we show that, in decreasing order, lipid markers representing fungi, Gram-negative bacteria, and Gram-positive bacteria have the highest relative abundances within honey bee colonies. Our lipid profiles reveal the presence of viable microbial communities in each of the six hive components sampled, with overall microbial community richness varying from lowest to highest in honey, comb, pupae, pollen, adults and propolis, respectively. Finally, microbial community lipid profiles were more similar when compared by component than by hive, location, or sampling year. Specifically, we found that individual hive components typically exhibited several dominant lipids and that these dominant lipids differ between components. Principal component and two-way clustering analyses both support significant grouping of lipids by hive component. Our findings indicate that in addition to the microbial communities present in individual workers, honey bee hives have resident microbial communities associated with different colony components.     

An information-theory analysis of task specialization among worker honey bees performing hive duties

Worker honey bees (Apis mellifera) performing field duties are known to possess individual task specializations. However, little evidence has been forthcoming about individual specializations among the younger pre-foraging worker bees performing hive duties. This paper reports results obtained from behavioural observations of worker bees in seven hives. An information-theory analysis of these data reveals that the divergence from independence (D₂) of worker bee identity and behavioural pattern performed has a low value in all of the experimental hives. Young worker bees performing hive duties therefore do not possess detectable individual specializations. Environmental and life-history considerations that may account for this difference in behaviour between field and hive worker bees are discussed.     

An ecological digest of the small hive beetle (Aethina tumida), a symbiont in honey bee colonies (Apis mellifera)

The small hive beetle (Aethina tumida Murray) is an endemic scavenger in colonies of western honey bee subspecies (Apis mellifera L.) inhabiting sub-Saharan Africa where it only occasionally damages host colonies. Such damage is usually restricted to weakened/diseased colonies or is associated with after absconding events (all bees, including the queen, leave the hive) due to behavioral resistance mechanisms of its host. In sharp contrast, the beetle has proven deleterious to honey bee colonies in introduced ranges of the United States and Australia. With this review we synthesize the existing data in a manner that allows us to discuss the beetle’s natural history from an ecological perspective. A thorough exploration of beetle ecology allows us to 1) illuminate the unique symbiotic relationship it and its host share and understand how this relationship is fostered, 2) place this relationship in context with those of other arthropods inhabiting social insect colonies, 3) understand its natural reliance on honey bee colonies, 4) predict its spread outside its native range, and 5) predict its effects on non-African honey bees and non-target species. Here we present an amalgamation of information that will contribute to a more thorough and appropriate understanding of not only small hive beetles as symbionts, but of social insect symbionts in general. Received 4 April 2005; revised 15 October 2005; accepted 18 October 2005.     

Viral Infection Affects Sucrose Responsiveness and Homing Ability of Forager Honey Bees,Apis mellifera L.

Honey bee health is mainly affected by Varroa destructor, viruses, Nosema spp., pesticide residues and poor nutrition. Interactions between these proposed factors may be responsible for the colony losses reported worldwide in recent years. In the present study, the effects of a honey bee virus, Israeli acute paralysis virus (IAPV), on the foraging behaviors and homing ability of European honey bees (Apis mellifera L.) were investigated based on proboscis extension response (PER) assays and radio frequency identification (RFID) systems. The pollen forager honey bees originated from colonies that had no detectable level of honey bee viruses and were manually inoculated with IAPV to induce the viral infection. The results showed that IAPV-inoculated honey bees were more responsive to low sucrose solutions compared to that of non-infected foragers. After two days of infection, around 10⁷ copies of IAPV were detected in the heads of these honey bees. The homing ability of IAPV-infected foragers was depressed significantly in comparison to the homing ability of uninfected foragers. The data provided evidence that IAPV infection in the heads may enable the virus to disorder foraging roles of honey bees and to interfere with brain functions that are responsible for learning, navigation, and orientation in the honey bees, thus, making honey bees have a lower response threshold to sucrose and lose their way back to the hive.     

Infectivity of DWV Associated to Flower Pollen: Experimental Evidence of a Horizontal Transmission Route

Deformed wing virus (DWV) is a honeybee pathogen whose presence is generally associated with infestation of the colony by the mite Varroa destructor, leading to the onset of infections responsible for the collapse of the bee colony. DWV contaminates bee products such as royal jelly, bee-bread and honey stored within the infected hive. Outside the hive, DWV has been found in pollen loads collected directly from infected as well as uninfected forager bees. It has been shown that the introduction of virus-contaminated pollen into a DWV-free hive results in the production of virus-contaminated food, whose role in the development of infected bees from virus-free eggs has been experimentally demonstrated. The aim of this study was twofold: (i) to ascertain the presence of DWV on pollen collected directly from flowers visited by honeybees and then quantify the viral load and (ii) determine whether the virus associated with pollen is infective. The results of our investigation provide evidence that DWV is present on pollen sampled directly from visited flowers and that, following injection in individuals belonging to the pollinator species Apis mellifera, it is able to establish an active infection, as indicated by the presence of replicating virus in the head of the injected bees. We also provide the first indication that the pollinator species Osmia cornuta is susceptible to DWV infection.     

Competition between honey bees and wild bees and the role of nesting resources in a nature reserve

The European honey bee exploits floral resources efficiently and may therefore compete with solitary wild bees. Hence, conservationists and bee keepers are debating about the consequences of beekeeping for the conservation of wild bees in nature reserves. We observed flower-visiting bees on flowers of Calluna vulgaris in sites differing in the distance to the next honey-bee hive and in sites with hives present and absent in the Lüneburger Heath, Germany. Additionally, we counted wild bee ground nests in sites that differ in their distance to the next hive and wild bee stem nests and stem-nesting bee species in sites with hives present and absent. We did not observe fewer honey bees or higher wild bee flower visits in sites with different distances to the next hive (up to 1,229 m). However, wild bees visited fewer flowers and honey bee visits increased in sites containing honey-bee hives and in sites containing honey-bee hives we found fewer stem-nesting bee species. The reproductive success, measured as number of nests, was not affected by distance to honey-bee hives or their presence but by availability and characteristics of nesting resources. Our results suggest that beekeeping in the Lüneburg Heath can affect the conservation of stem-nesting bee species richness but not the overall reproduction either of stem-nesting or of ground-nesting bees. Future experiments need control sites with larger distances than 500 m to hives. Until more information is available, conservation efforts should forgo to enhance honey bee stocking rates but enhance the availability of nesting resources.     

The scent of the waggle dance

The waggle dance of honey bee (Apis mellifera L.) foragers communicates to nest mates the location of a profitable food source. We used solid-phase microextraction and gas chromatography coupled with mass spectrometry to show that waggle-dancing bees produce and release two alkanes, tricosane and pentacosane, and two alkenes, Z-(9)-tricosene and Z-(9)-pentacosene, onto their abdomens and into the air. Nondancing foragers returning from the same food source produce these substances in only minute quantities. Injection of the scent significantly affects worker behavior by increasing the number of bees that exit the hive. The results of this study suggest that these compounds are semiochemicals involved in worker recruitment. By showing that honey bee waggle dancers produce and release behaviorally active chemicals, this study reveals a new dimension in the organization of honey bee foraging.     

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.     

Small Hive Beetles are Facultative Predators of Adult Honey Bees

Foraging animals can choose to act as predators or not depending on the level of defensiveness of the potential prey. This requires prior evaluation of prey defensiveness, which can be variable, e.g. young insects are usually less able to defend themselves. Here we show that small hive beetles, Aethina tumida, which are scavengers and parasites of honey bee, Apis mellifera, colonies, are facultative predators of young adult host workers. Adult female beetles mounted and attacked young workers more often than their older nestmates, indicating that the beetle is assessing the defensiveness of the host and is adjusting its behaviour accordingly. Since adult female beetles need proteins to activate their ovaries, predation on defenceless young alive host workers offers another rewarding food source, which can obviously not be exploited by beetle larvae. In conclusion, adult small hive beetles seem to be able to assess the trade-off between safety and food reward.     

Insight into probiotic properties of lactic acid bacterial endosymbionts of Apis mellifera L. derived from the Polish apiary

Taking into account that fructophilic lactic acid bacteria (FLAB) can play an important role in the health of honey bees and can be used as probiotics, phenotypic properties of probiotic interest of Lactobacillus kunkeei (12 strains) and Fructobacillus fructossus bacteria (2 strains), isolated from Apis mellifera gastrointestinal tract, have been studied. We have evaluated survival of tested FLAB in honey bee gut, their susceptibility to antibiotics (ampicillin, erythromycin, tylosin), cell surface hydrophobicity, auto-aggregation ability, co-aggregation with model pathogenic bacteria, biofilm formation capacity, and effect of studied FLAB, added to sucrose syrup bee diet, on longevity of honey bees. The tested FLAB exhibited good gastrointestinal tract tolerance and high antibiotic susceptibility, which are important criteria in the screening of probiotic candidates. It was also found that all FLAB studied have high cell surface hydrophobicity and fulfil next selection criterion for their use as probiotics. Symbionts of A. mellifera showed also auto- and co-aggregation capacities regarded as valuable features for biofilm formation and inhibition of pathogens adhesion to the bee gut cells. Biofilm-development ability is a desired characteristic of probiotic lactic acid bacteria. As indicated by quantitative crystal violet-stained microplate assay and confocal laser scanning microscopy imaging, all studied A. mellifera gut isolates exhibit a biofilm positive phenotype. Moreover, it was also documented, on honey bees kept in cages, that supplementation of A. mellifera sucrose diet with FLAB decreases mortality and improves significantly longevity of honey bees. Presented research showed that A. mellifera FLAB symbionts are good candidates for application as probiotics.     

Confinement Behavior of Cape Honey Bees (Apis mellifera capensis Esch.) in Relation to Population Densities of Small Hive Beetles (Aethina tumida Murray)

We quantified the effects of increasing small hive beetle (Aethina tumida Murray) populations on guarding behavior of Cape honey bees (Apis mellifera capensis, an African subspecies). We found more confinement sites (prisons) at the higher (50 beetles per colony) rather than lower (25 beetles per colony) beetle density. The number of beetles per prison did not change with beetle density. There were more guard bees per beetle during evening than morning. Neither guard bee nor beetle behavior varied with beetle density or over time. Forty-six percent of all beetles were found among the combs at the low beetle density and this increased to 58% at the higher one. In neither instance were beetles causing depredation to host colonies. Within the limits of the experiment, guarding behavior of Cape honey bees is relatively unaffected by increasing beetle density (even if significant proportions of beetles reach the combs).     

A new threat to honey bees, the parasitic phorid fly Apocephalus borealis

Honey bee colonies are subject to numerous pathogens and parasites. Interaction among multiple pathogens and parasites is the proposed cause for Colony Collapse Disorder (CCD), a syndrome characterized by worker bees abandoning their hive. Here we provide the first documentation that the phorid fly Apocephalus borealis, previously known to parasitize bumble bees, also infects and eventually kills honey bees and may pose an emerging threat to North American apiculture. Parasitized honey bees show hive abandonment behavior, leaving their hives at night and dying shortly thereafter. On average, seven days later up to 13 phorid larvae emerge from each dead bee and pupate away from the bee. Using DNA barcoding, we confirmed that phorids that emerged from honey bees and bumble bees were the same species. Microarray analyses of honey bees from infected hives revealed that these bees are often infected with deformed wing virus and Nosema ceranae. Larvae and adult phorids also tested positive for these pathogens, implicating the fly as a potential vector or reservoir of these honey bee pathogens. Phorid parasitism may affect hive viability since 77% of sites sampled in the San Francisco Bay Area were infected by the fly and microarray analyses detected phorids in commercial hives in South Dakota and California's Central Valley. Understanding details of phorid infection may shed light on similar hive abandonment behaviors seen in CCD.     

Structural and functional differences in the antennal olfactory system of worker honey bees of Apis mellifera and Apis cerana

Olfactory cues are important sensory modalities on individual discrimination, perception, and efficient orientation to food sources in most insects. In honey bees, which are well known as eusocial insects, olfactory cues are mainly used to maintain a colony. Although much research has been reported on olfactory systems in honey bee olfaction, little is known about the differences between two major honey bee species, the European honey bee Apis mellifera and the Asian honey bee Apis cerana. In order to understand the differences of olfactory characteristics in the two species, we compared the distribution of sensory hairs on the antennae and antennal olfactory responses, using electron microscopy, electrophysiological recording and molecular expression level of odorant receptors. Our present study demonstrated that the antennae of A. cerana have more olfactory sensilla than A. mellifera, responding more strongly to various floral volatile compounds. At the molecular level, olfactory co-receptor (Orco), which makes heterodimers with other conventional olfactory receptors, is more abundantly expressed in the antenna of A. cerana than of A. mellifera. These findings extend our understanding of the olfactory systems and behavioral responses to various ecological and biological signals in two closely related honey bee species.     

Pollen diets and niche overlap of honey bees and native bees in protected areas

The decline of both managed and wild bee populations has been extensively reported for over a decade now, with growing concerns amongst the scientific community. Also, evidence is growing that both managed and feral honey bees may exacerbate threats to wild bees. In Australia, there are over 1600 native bee species and introduced European honey bees (Apis mellifera) have established throughout most landscapes. There is a major gap in knowledge of the interactions between honey bees and native bees in Australian landscapes, especially floral resource use.Here we report on the pollen diets of wild bees in protected areas of coastal heathland, an ecosystem characterised by mass flowering in late winter and spring. We sampled bees within three sites and DNA metabarcoding was used to compare the pollen diets of honey bees and native bees. We recorded 2, 772 bees in total, with 13 genera and 18 described species identified. Apis mellifera was the most common species across all locations, accounting for 42% of all bees collected. Native bee genera included eusocial Tetragonula (stingless bees) (37%), and semi-social Exoneura and Braunsapis (19.8% combined). Metabarcoding data revealed both Tetragonula and honey bees have wide foraging patterns, and the bipartite network overall was highly generalised (H₂’ = 0.24). Individual honey bees carried pollen of 7–29 plant species, and significantly more species than all other bees. We found niche overlap in the diets of honey bees and native bees generally (0.42), and strongest overlap with stingless bees (0.70) and species of Braunsapis (0.62). A surprising finding was that many species carried pollen from Restionaceae and Cyperaceae, families generally considered to be predominantly wind-pollinated in Australia. Our study showed introduced honey bee use of resources overlaps with that of native bees in protected heathlands, but there are clear differences in their diet preferences.     

Longevity and reproductive success of Aethina tumida (Coleoptera: Nitidulidae) fed different natural diets

The longevity and reproductive success of newly emerged, unfed adult Aethina tumida Murray assigned different diets (control = unfed; honey-pollen; honey; pollen; empty brood comb; bee brood; fresh Kei apples; and rotten Kei apples) were determined. Longevity in honey-fed small hive beetle adults (average maximum: 167 d) was significantly higher than on other diets. Small hive beetles fed empty brood comb lived significantly longer (average maximum: 49.8 d) than unfed beetles (average maximum: 9.6 d). Small hive beetle offspring were produced on honey-pollen, pollen, bee brood, fresh Kei apples, and rotten Kei apples but not on honey alone, empty brood comb, or in control treatments. The highest reproductive success occurred in pollen fed adults (1773.8 +/- 294.4 larvae per three mating pairs of adults). The data also show that A. tumida can reproduce on fruits alone, indicating that they are facultative parasites. The pupation success and sex ratio of small hive beetle offspring were also analyzed. Larvae fed pollen, honey-pollen, or brood had significantly higher pupation success rates of 0.64, 0.73, and 0.65 respectively than on the other diets. Sex ratios of emerging adults fed diets of pollen or brood as larvae were significantly skewed toward females. Because small hive beetle longevity and overall reproductive success was highest on foodstuffs located in honey bee colonies, A. tumida are efficient at causing large-scale damage to colonies of honey bees resulting in economic injury for the beekeeper. Practical considerations for the control of A. tumida are briefly discussed.     

Red mason bees cannot compete with honey bees for floral resources in a cage experiment

Intensive beekeeping to mitigate crop pollination deficits and habitat loss may cause interspecific competition between bees. Studies show negative correlations between flower visitation of honey bees (Apis mellifera) and wild bees, but effects on the reproduction of wild bees were not proven. Likely reasons are that honey bees can hardly be excluded from controls and wild bee nests are generally difficult to detect in field experiments. The goal of this study was to investigate whether red mason bees (Osmia bicornis) compete with honey bees in cages in order to compare the reproduction of red mason bees under different honey bee densities. Three treatments were applied, each replicated in four cages of 18 m³ with 38 red mason bees in all treatments and 0, 100, and 300 honey bees per treatment with 10–20% being foragers. Within the cages, the flower visitation and interspecific displacements from flowers were observed. Niche breadths and resource overlaps of both bee species were calculated, and the reproduction of red mason bees was measured. Red mason bees visited fewer flowers when honey bees were present. Niche breadth of red mason bees decreased with increasing honey bee density while resource overlaps remained constant. The reproduction of red mason bees decreased in cages with honey bees. In conclusion, our experimental results show that in small and isolated flower patches, wild bees can temporarily suffer from competition with honey bees. Further research should aim to test for competition on small and isolated flower patches in real landscapes.