Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida)

Abstract.  1. The small hive beetle, Aethina tumida , is a parasite of honeybee ( Apis mellifera ) colonies native to sub-Saharan Africa and has become an invasive species. In North America the beetle is now sympatric with bumblebees, Bombus , not occurring in its native range. Laboratory studies have shown that small hive beetles can reproduce in bumblebee colonies but it was not known whether infestations occur in the field.
2. For the first time, infestation of bumblebee colonies by small hive beetles was investigated in the field. Commercial Bombus impatiens colonies ( n = 10) were installed in proximity to infested apiaries. Within 8 weeks, all colonies that were alive in the 5-week observation period ( n = 9) became naturally infested with adult small hive beetles and successful small hive beetle reproduction occurred in five colonies.
3. In four-square choice tests, the beetles were attracted to both adult bumblebee workers and pollen from bumblebee nests, suggesting that these odours may serve as cues for host finding.
4. The data indicate that bumblebee colonies may serve as alternative hosts for small hive beetles in the field. To foster the conservation of these essential native pollinators, investigations on the actual impact of small hive beetles on wild bumblebee populations are suggested.     

Social encapsulation of the small hive beetle (<Emphasis Type="Italic">Aethina tumida</Emphasis> Murray) by European honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

Summary European and African subspecies of honeybees (Apis mellifera L.) utilize social encapsulation to contain the small hive beetle (Aethina tumida Murray), a honeybee colony scavenger. Using social encapsulation, African honeybees successfully limit beetle reproduction that can devastate host colonies. In sharp contrast, European honeybees often fail to contain beetles, possibly because their social encapsulation skills may be less developed than those of African honeybees. In this study, we quantify beetle and European honeybee behaviours associated with social encapsulation, describe colony and time (morning and evening) differences in these behaviours (to identify possible circadian rhythms), and detail intra-colonial, encapsulated beetle distributions. The data help explain the susceptibility of European honeybees to depredation by small hive beetles. There were significant colony differences in a number of social encapsulation behaviours (the number of beetle prisons and beetles per prison, and the proportion of prison guard bees biting at encapsulated beetles) suggesting that successful encapsulation of beetles by European bees varies between colonies. We also found evidence for the existence of circadian rhythms in small hive beetles, as they were more active in the evening rather than morning. In response to increased beetle activity during the evening, there was an increase in the number of prison guard bees during evening. Additionally, the bees successfully kept most (~93%) beetles out of the combs at all times, suggesting that social encapsulation by European honeybees is sufficient to control small populations of beetles (as seen in this study) but may ultimately fail if beetle populations are high.Received 20 January 2003; revised 21 April 2003; accepted 29 April 2003.     

Adaptive behaviour of honeybees (Apis mellifera) toward beetle invaders exhibiting various levels of colony integration

Social bees generally host fewer nest invaders than do ants and termites. This is potentially explained by the adaptive defensive strategies of host bees when faced with nest invaders exhibiting various levels of colony integration (based on adaptations to the nest habitat and frequency of nest inhabitation). In the present study, experiments are performed to determine the behaviour at the nest entrance of European honeybee guards Apis mellifera L. (Hymenoptera: Apidae) toward beetle invaders of various levels of behavioural integration into colonies. The species used to test this include Aethina tumida Murray (Coleoptera: Nitidulidae), which is regarded as a highly integrated, unwelcome guest (synechthran) or true guest (symphile); Lobiopa insularis Laporte (Coleoptera: Nitidulidae) and Epuraea luteola Erichson (Coleoptera: Nitidulidae) that are accidentals; and Carpophilus humeralis Fabricius (Coleoptera: Nitidulidae), Carpophilus hemipterus L. (Coleoptera: Nitidulidae) and Tribolium castaneum Herbst (Coleoptera: Tenebrionidae), all of which are species that are not integrated into honeybee colonies. The responses of guard bees to a control bead also are noted. In general, bees ignore T. castaneum and E. luteola to a greater extent than other beetle species. Bees make contact with the black glass bead (a non‐aggressive behaviour) more than they do all beetle species. Bees treat A. tumida more defensively than they treat any other beetle species and the level of bee defensiveness varies by colony. These data suggest an adaptive heightened defensive response by bees toward the most integrated colony intruder but a significantly reduced level of response toward invaders representing all other levels of colony integration.     

Colony contact contributes to the diversity of gut bacteria in bumblebees (Bombus terrestris)

Social bees, like honeybees and bumblebees, have a close contact with nest mates of different developmental stages and generations. This could enhance bacterial transfer between nest mates and offers opportunities for direct transfer of symbionts from one generation to the next, resulting in a stable host specific gut microbiota. Gut symbionts of honeybees and bumblebees have been suggested to contribute in digestion and protection against parasites and pathogens. Here we studied the impact of contact with the bumblebee colony on the colonization potential of the bacterial families (i.e., Neisseriaceae, Orbaceae, Lactobacillaceae and Bifidobacteriaceae) occurring in the gut of adult bumblebees (Bombus terrestris). Bacterial profiles of the gut microbiota of B. terrestris were determined based on the hypervariable V4 region of the 16S rRNA using paired‐end Illumina sequencing. In our experiments, we created different groups in which we gradually reduced the contact with nest mates and hive material. We made 3 observations: (i) reducing the contact between the colony and the bumblebee during adult life resulted in a significant drop in the relative abundance of Lactobacillus bombicola and Lactobacillus bombi; (ii) Bifidobacteriaceae required contact with nest mates to colonize the gut of B. terrestris and a significant lower bacterial diversity was observed in bumblebees that were completely excluded from colony contact during the adult life; (iii) Snodgrassella and Gilliamella were able to colonize the gut of the adult bumblebee without any direct contact with nest mates in the adult life stage. These results indicate the impact of the colony life on the diversity of the characteristic bumblebee gut bacteria.     

The Impact of Recent Queenloss and Colony Pheno-type on the Removal of Small Hive Beetle (Aethina tumida Murray) Eggs and Larvae by African Honeybee Colonies (Apis mellifera capensis Esch.)

The removal of small hive beetle [=SHB] eggs and larvae was studied in queenright and recently queenless Cape honeybee, Apis mellifera capensis, colonies over a range of phenotypes. The overall removal efficiency was not influenced by phenotypes or queenstate, because all introduced eggs and larvae were removed within 24 hours. Queenless colonies removed them merely slower than queenright ones. The latter ones rejected up to 300 larvae within one hour. However, colonies undergoing preparation for absconding did not completely remove SHB offspring, suggesting that removal efficiency was reduced. Since even small and recently queenless colonies effectively removed immature SHB, and no differences in the overall efficiency was found compared to A. m. scutellata we conclude that this defense behavior is well developed in African honeybees.     

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.     

The ectoparasitic mite Tropilaelaps mercedesae (Acari, Laelapidae) as a vector of honeybee viruses

The ectoparasitic mites Varroa destructor and Tropilaelaps mercedesae share life history traits and both infect honeybee colonies, Apis mellifera. Since V. destructor is a biological vector of several honeybee viruses, we here test whether T. mercedesae can also be infected and enable virus replication. In Kunming (China), workers and T. mercedesae mites were sampled from three A. mellifera colonies, where workers were exhibiting clinical symptoms of deformed wing virus (DWV). We analysed a pooled bee sample (15 workers) and 29 mites for the presence of Deformed wing virus (DWV), Black queen cell virus (BQCV), Sacbrood virus (SBV), Kashmir bee virus (KBV), Acute bee paralysis virus (ABPV), and Chronic bee paralysis virus (CBPV). Virus positive samples were analysed with a qPCR. Only DWV +RNA was found but with a high titre of up to 10⁸ equivalent virus copies per mite and 10⁶ per bee. Moreover, in all DWV positive mites (N= 12) and in the bee sample virus–RNA was also detected using RT-PCR and tagged RT-PCR, strongly suggesting virus replication. Our data show for the first time that T. mercedesae may be a biological vector of DWV, which would open a novel route of virus spread in A. mellifera. Received 6 June 2008; revised 14 August 2008; accepted 10 September 2008.     

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).     

How <Emphasis Type="Italic">Apis mellifera</Emphasis> Behaves with its Invasive Hornet Predator <Emphasis Type="Italic">Vespa velutina</Emphasis>?

Invasive species are now recognized as a major cause of native biodiversity loss worldwide. In the current deleterious context for pollinators, the invasive yellow-legged hornet, Vespa velutina, represents an additional threat to the domestic honeybee, Apis mellifera, in Europe. Therefore, understanding the impact of this predator on honeybee colonies is of major importance. In the present study, we tried to assess the impact of V. velutina on the honeybee foraging and defence behaviour based on the video monitoring of two hives. Balling behaviour is reported here for the first time under natural conditions in A. mellifera against V. velutina in Europe. Although these results are preliminary and should be carefully considered, we found that the number of hornets impacted honeybee foraging and defence behaviours. More defensive behaviours were notified in the hive, which survives slightly longer. This may suggest that selecting for more defensive colonies may provide an interesting perspective.     

Estimating the genetic variance of group characters: social behaviour of honeybees (Apis mellifera L.)

Summary A new approach is presented to estimate the genetic variance of social behaviour of groups. Honeybees (Apis mellifera L.) are used as an example for highly social organisms. Most characters of economic importance strongly rely on collective group characters of honeybee colonies. The average relatedness between small groups of workers of one honeybee colony can be estimated using a discrete multinomial distribution. The genetic variance of a social behaviour (alarm behaviour) of groups of honeybee workers is estimated with the intraclass correlation between groups within a colony. In two populations tested, the coefficient of genetic determination was high (0.96–0.98) indicating that the metabolic bio-assay used was only weakly affected by environmental effects.     

The relationship between the abundances of bumblebees and honeybees in a native habitat

Abstract. 1. The western honeybee, Apis mellifera, has been introduced to many parts of the world and is sometimes purported to be detrimental to native bees because it reduces their food base. It is seldom viewed in this light in Europe; however, when beekeepers maintain very high bee densities, the species could also be displacing insects in its native European range by reducing the resource base. 2. In England, populations of bumblebees (Bombus Latr. Hym.) have been decreasing both in terms of diversity and abundance, mainly because of a loss of habitat resulting from agricultural intensification. The impact of competition from other flower feeders is largely unknown. 3. Nineteen dry lowland heaths in southern England were sampled once for honeybees and bumblebees. Honeybee abundance varied from 4 to 81 bees per 100 m² (mean = 30.89, median = 23), whereas bumblebees varied from 2 to 17 individuals per 100 m² (mean = 8.26, median = 7), belonging to between one and five species. There was a negative association between honeybee and bumblebee abundance but there was no apparent relationship between honeybee abundance and bumblebee diversity. 4. The Bray–Curtis coefficient was used to compare the similarity in honeybee and bumblebee floral host breadth at these 19 sites. The coefficient was negatively associated with honeybee abundance: thus where honeybees were most abundant, bumblebees were fewer and/or foraged on different flower species. 5. Foraging host breadth was also examined at four heathlands over a field season (April to September). No association between honeybee abundance and foraging host breadth was found for short‐tongued bees, although there was some evidence for a change in floral host breadth for long‐tongued bees. 6. It is concluded that the impact of honeybees on bumblebees is complex. Although competition between the two species cannot be ruled out, it is perhaps equally likely that bumblebees decline in response to other factors, and that honeybees move independently of this decline.     

Preparation for disturbance-induced absconding of Cape honeybee colonies (Apis mellifera capensis Esch.)

African honeybees, Apis mellifera, are characterised by frequent disturbance-induced absconding. However, the effectiveness in preparation before such disturbance-induced absconding has not been rigorously quantified yet. We investigated the effectiveness of preparation for disturbance-induced absconding by evaluating colony phenotypes prior to and after absconding in ten colonies of the Cape honeybee, A. m. capensis. Seven non-absconding colonies at the same apiary were used as controls. While seven absconded colonies left neither stores nor brood behind, three colonies abandoned only a small area of honey, pollen, open or capped brood. At the end of the observations, the control colonies still had pollen and honey stores and brood. The mean reduction rate between a major disturbance and the absconding event was 0.052 ± 0.018 cm² stores and open brood per worker per day. Our results demonstrate that disturbance-induced absconding can also occur with preparation, if the disturbance is not highly destructive and enough time for preparation is available. We conclude that Cape honeybee colonies can show a considerable high effectiveness in their preparation before disturbance-induced absconding, which limits the loss of colony resources. In light of the general high mobility of African honeybee colonies such an efficient behaviour is probably adaptive. Received 22 December 2004; revised 3 June 2005; accepted 13 June 2005.     

Food and reproductive strategies of the myrmecophilous staphylinid beetleHomoeusa acuminata (aleocharinae) on the foraging trails of its host antLasius fuliginosus (Hymenoptera: Formicidae)

Summary The trail following behaviour of the adult myrmecophilous beetleHomoeusa acuminata on the foraging trails on the host antLasius fuliginosus was examined in June and all the observed behaviours were quantified. The beetle appears as a food robber, using the stowaway behaviour which consists of attaching itself to prey transported by ants to the nest. Foraging trails are also used by the beetles as a meeting place for mating. However, the beetle does not enter into the nest and appears as a symbiont poorly integrated in the social life of its host.     

Hive debris counts in honeybee colonies: a method to estimate the size of small populations and rate of growth of the miteVarroa jacobsoni Oud. (Mesostigmata: Varroidae)

Fifteen honeybee colonies (Apis mellifera L.) infested with the ectoparasiteVarroa jacobsoni Oud. were monitored for the number of mites falling to the bottom of the hive. Mites in the debris were counted periodically on the plastic sheet on which they were collected. Two months later, colonies were treated with an acaricide to determine mite population. A high positive correlation was found between the number of mites collected in the hive debris over different periods and the final population size. Based on this correlation, it was possible to use hive debris counts to predict the degree of infestation. Furthermore, counting fallen mites over a period of two months, followed by an acaricide treatment, might be a useful method of estimating the rate of growth ofV. jacobsoni in honeybee colonies.     

The Value of Uncropped Field Margins For Foraging Bumblebees

The intensification of agriculture has led to declines in species diversity and abundance within groups of certain flora and fauna. Bumblebees (Bombus spp.) are one group where a decline has been documented, and it is thought to be attributable to a decrease in forage resources and potential nest sites. As bumblebees play an important role in the pollination of many entomophilous crops, this decline could impact on agricultural productivity. We examined the role of naturally regenerated field margins in providing forage plants on land where nectar resources are otherwise impoverished. The following question was addressed – Are naturally regenerated unsprayed field margins more attractive to foraging bumblebees and honeybees than cropped field margins managed as conservation headlands? Significantly more bees visited naturally regenerated field margins than cropped field margins. Honeybees (Apis mellifera), Bombus terrestris, and Bombus lapidarius were the most commonly observed bee species. Different wildflower species within the naturally regenerated margins varied greatly in relative number of visits received, and bumblebee species were found to prefer different flower species to honeybees. The potential role that naturally regenerated field margins could play in the conservation of bumblebee species, and the implications for other species of flora and fauna, are discussed.     

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.     

Nest defence in a stingless bee: What causes fighting swarms in Trigona carbonaria (Hymenoptera, Meliponini)?

The Australian stingless bee Trigona carbonaria sometimes displays a striking collective behaviour, known as a ‘fighting swarm’ in which thousands of workers fight and die. Molecular analysis of eight naturally-occurring fights showed they almost always comprise just two colonies, one of which is located within 2 m of the fight. Fighting swarms were experimentally triggered by manipulating colonies so that they received non-nestmate workers. Combined, our investigations suggest that T. carbonaria fighting swarms arise as a collective defence of the nest from conspecific invasion (e.g. robbery or nest usurpation) Received 16 November 2007; revised 31 March 2008; accepted 1 July 2008.     

Diploid male production in a rare and locally distributed bumblebee, Bombus florilegus (Hymenoptera, Apidae)

The European bumblebee B. terrestris was recently introduced in Japan for agricultural purposes and has now become naturalized. The naturalization of this exotic species may have great detrimental effects on closely related native Japanese bumblebees. The Japanese bumblebee Bombus florilegus is a rare and locally distributed species found in the Nemuro Peninsula of Hokkaido, Japan. In order to assess its population genetics, we estimated the genetic structure of B. florilegus in 16 breeding colonies (queen, workers, and males) and 20 foraging queens by analyzing microsatellite DNA markers. Of the 36 queens analyzed by genotyping and dissection, 32 had been inseminated by a male. The remaining 4 had not been inseminated at all. Of the 4 nonmated queens, one was triploid. Diploid males were found in 4 breeding colonies. Based on the microsatellite data, it appears that B. florilegus has low reproductive success. Since matched mating and nonmating within local populations are high, the extinction risk is correspondingly higher. Our results suggest that conservation of the Japanese B. florilegus is required in order to protect it from both habitat destruction and the naturalization of alien species. Received 19 July 2007; revised 13 October 2007; accepted 15 October 2007.     

Worldwide migration of parasitic mites as a result of bumblebee commercialization

We investigated the status of infestation by a tracheal mite, Locustacarus buchneri, in natural populations of a Japanese native bumblebee species, Bombus hypocrita, collected on Hokkaido Island and in the Aomori prefecture between 1997 and 2001. We also investigated mite infestation in commercial colonies of the European bumblebee, Bombus terrestris, imported from the Netherlands and Belgium, and the Japanese native species, B. ignitus, imported from the Netherlands, between 1997 and 2001. We detected mites in natural populations of the two B. hypocrita subspecies and in the commercial colonies. Analysis of variations in 535 bp sequences of the mitochondrial cytochrome oxidase subunit 1 (CO1) gene showed that the mite haplotypes in the native populations and in the imported colonies did not overlap in 1997–1999, but in 2000–2001 some mites possessing European CO1 haplotypes were detected in the natural populations of Japanese native bumblebees. In addition, many mites possessing Japanese haplotypes were detected in the imported commercial colonies from Europe. Considering the fact that the Japanese native bumblebees, B. hypocrita, were once exported to Europe for commercialization, these results suggest that bumblebee commercialization has caused overseas migration and cross-infestation of parasitic mites among natural and commercial colonies. However, because the Japanese and European CO1 haplotypes were closely related, there was a possibility that the European haplotypes found in the mites in the Hokkaido Island revealed native variation. To clarify the status of mite invasion, further detailed analysis of genetic variation of the mite, using other genetic markers on additional samples, need to be performed.