Behavioural responses of the small hive beetle to volatile components of fermenting honeybee hive products

The small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae), is a significant pest of managed honeybees in the USA and eastern Australia. The beetle damages hives by feeding on hive products and leaving behind fermented wastes. The beetle is consistently associated with the yeast Kodamaea ohmeri (Etchells & Bell) Yamada et al. (Saccharomycetales: Metschnikowiaceae), and this yeast is the presumed agent of the fermentation. Previous work has noted that the small hive beetle is attracted to volatiles from hive products and those of the yeast K. ohmeri. In this study, we investigated how the volatile compounds from the fermenting hive products change depending upon the source of the hive material and also how these volatiles change through time. We used gas chromatography–mass spectrometry and choice‐test behavioural assays to investigate these changes using products sampled from apiaries across the established range of the beetle in eastern Australia. The starting hive products significantly affected the volatile composition of fermenting hive products, and this composition varied throughout time. We found 61.7% dissimilarity between attractive and non‐attractive fermenting hive products, and identified individual compounds that characterise each of these groups. Eleven of these individual compounds were then assessed for attractiveness, as well as testing a synthetic blend in the laboratory. In the laboratory bioassay, 82.1 ± 0.02% of beetles were trapped in blend traps. These results have strong implications for the development of an out‐of‐hive attractant trap to assist in the management of this invasive pest.     

Increased attractiveness of honeybee hive product volatiles to adult small hive beetle,Aethina tumida,resulting from small hive beetle larval infestation

The small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae), is a recent but significant pest of honeybee [Apis mellifera L. (Hymenoptera: Apidae)] hives in various regions throughout the world, including Eastern Australia. The larval stage of this beetle damages hives when they feed on brood, pollen, and honeycomb, leaving behind fermented wastes. In cases of extreme damage, hives collapse and are turned to an odorous mass of larvae in fermenting hive products. The yeast Kodamaea ohmeri (Etchells & Bell) Yamada et al. (Ascomycota) has been consistently isolated from the fermenting material as well as each life stage of this beetle. Various studies have noted that the small hive beetle is attracted to volatiles from hive products and those of the yeast K. ohmeri, although earlier studies have not used naturally occurring hive products as their source of fermentation. This study investigated changes through time in the attractiveness of natural honeybee hive products to the small hive beetle as the hive products were altered by the action of beetle larvae and fermentation by K. ohmeri. We used gas chromatography‐mass spectrometry and choice‐test behavioural assays to investigate these changes using products sampled from three apiaries. Attractiveness of the fermenting hive products (‘slime’) increased as fermentation progressed, and volatile profiles became more complex. Fermenting hive products remained extremely attractive for more than 30 days, significantly longer than previous reports. These results have strong implications for the development of an external attractant trap to assist in the management of this invasive pest.     

Hit‐and‐run trophallaxis of small hive beetles

Some parasites of social insects are able to exploit the exchange of food between nestmates via trophallaxis, because they are chemically disguised as nestmates. However, a few parasites succeed in trophallactic solicitation although they are attacked by workers. The underlying mechanisms are not well understood. The small hive beetle (=SHB), Aethina tumida, is such a parasite of honey bee, Apis mellifera, colonies and is able to induce trophallaxis. Here, we investigate whether SHB trophallactic solicitation is innate and affected by sex and experience. We quantified characteristics of the trophallactic solicitation in SHBs from laboratory‐reared individuals that were either bee‐naïve or had 5 days experience. The data clearly show that SHB trophallactic solicitation is innate and further suggest that it can be influenced by both experience and sex. Inexperienced SHB males begged more often than any of the other groups had longer breaks than their experienced counterparts and a longer soliciting duration than both experienced SHB males and females, suggesting that they start rather slowly and gain more from experience. Successful experienced females and males were not significantly different from each other in relation to successful trophallactic interactions, but had a significantly shorter soliciting duration compared to all other groups, except successful inexperienced females. Trophallactic solicitation success, feeding duration and begging duration were not significantly affected by either SHB sex or experience, supporting the notion that these behaviors are important for survival in host colonies. Overall, success seems to be governed by quality rather than quantity of interactions, thereby probably limiting both SHB energy investment and chance of injury (<1%). Trophallactic solicitation by SHBs is a singular example for an alternative strategy to exploit insect societies without requiring chemical disguise. Hit‐and‐run trophallaxis is an attractive test system to get an insight into trophallaxis in the social insects.     

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.     

Keeping a low profile: small hive beetle reproduction in African honeybee colonies

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Bees and flowers: How to feed an invasive beetle species

Invasive species may exploit a wide range of food sources, thereby fostering their success and hampering mitigation, but the actual degree of opportunism is often unknown. The small hive beetle (SHB), Aethina tumida, is a parasite of honeybee colonies endemic to sub‐Saharan Africa. SHBs have now spread on all habitable continents and can also infest colonies of other social bees. To date, the possible role of solitary bee nests as alternative hosts is unknown. Similarly, flowers as possible alternative food sources are not well understood. Here, we show that SHBs can complete an entire life cycle in association with nests of solitary bees Megachile rotundata. The data also show that flowers can serve as alternative food sources. These results support the opportunistic nature of this invasive species, thereby generating further obstacles for mitigation efforts in the field. It also suggests that SHB invasions may result in more serious consequences for endemic bee fauna than previously thought. This provides further motivation to slow down the global spread of this pest, and to improve its management in areas, where it is established.     

Behavioral defense strategies of the stingless bee, <Emphasis Type="Italic">Austroplebeia australis</Emphasis>, against the small hive beetle, <Emphasis Type="Italic">Aethina tumida</Emphasis>

Small hive beetle, Aethina tumida Murray, is a parasite of social bee colonies and has become an invasive species, raising concern of the potential threat to native pollinators in its new ranges. Here, we report the defensive behavior strategies used by workers of the Australian stingless bee, Austroplebeia australis Friese, against the small hive beetle. A non-destructive method was used to observe in-hive behavior and interactions between bees and different life stages of small hive beetle (egg, larva, and adult). A number of different individual and group defensive behaviors were recorded. Up to 97% of small hive beetle eggs were destroyed within 90 min of introduction, with a significant increase in temporal rate of destruction between the first and subsequent introductions. A similar result was recorded for 3-day-old small hive beetle larvae, with an increased removal rate from 62.5 to 92.5% between the first and second introductions. Of 32 adult beetles introduced directly into the 4 colonies, 59% were ejected, with the remainder being entombed alive in hives within 6 h. Efficiency of ejection also significantly increased between the first and third introductions. Our observations suggest that A. australis colonies, despite no previous exposure to this exotic parasite, have well developed hive defences that are likely to minimize entry and survival of small hive beetles.     

Olfactory responses of Aethina tumida murray (Coleoptera: Nitidulidae) to some major volatile compounds from hive materials and workers of Apis mellifera

The small hive beetle (Aethina tumida Murray) is an invasive pest affecting honey bee colonies. The beetles are known to be attracted to volatiles from hive products and honey bees like Apis mellifera L. Previously we reported the presence of five major compounds from the volatile extracts of hive materials; ethyl linolenate and ethyl palmitate from pollen dough, oleamide and tetracosane in fermenting honey, and oleamide and 5-methyl-2-phenyl-1H-indole from A. mellifera worker bees. This study tested the attractiveness of the aforementioned five volatile organic compounds to small hive beetles (SHB) by Y-tube olfactometric bioassay. Ethyl linolenate was highly attractive to both male and female adults of SHB. Ethyl palmitate was attractive to SHB only at higher concentration (0.01–01 mg/ml). Interestingly, tetracosane, 5-methyl-2-phenyl-1H-indole and oleamide were repellent for SHB of both sexes, but ethyl linolenate and ethyl palmitate as components of honey bee brood pheromone attracted SHB. The results highlight that SHB differentially utilizes volatile chemicals from hive materials and honey bees as cues to locate honey bee hives.     

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.     

Global warming promotes biological invasion of a honey bee pest

Climate change and biological invasions are two major global environmental challenges. Both may interact, e.g. via altered impact and distribution of invasive alien species. Even though invasive species play a key role for compromising the health of honey bees, the impact of climate change on the severity of such species is still unknown. The small hive beetle (SHB, Aethina tumida, Murray) is a parasite of honey bee colonies. It is endemic to sub‐Saharan Africa and has established populations on all continents except Antarctica. Since SHBs pupate in soil, pupation performance is governed foremost by two abiotic factors, soil temperature and moisture, which will be affected by climate change. Here, we investigated SHB invasion risk globally under current and future climate scenarios. We modelled survival and development time during pupation (=pupal performance) in response to soil temperature and soil moisture using published and novel experimental data. Presence data on SHB distribution were used for model validation. We then linked the model with global soil data in order to classify areas (resolution: 10 arcmin; i.e. 18.6 km at the equator) as unsuitable, marginal and suitable for SHB pupation performance. Under the current climate, the results show that many areas globally yet uninvaded are actually suitable, suggesting considerable SHB invasion risk. Future scenarios of global warming project a vehement increase in climatic suitability for SHB and corresponding potential for invasion, especially in the temperate regions of the Northern hemisphere, thereby creating demand for enhanced and adapted mitigation and management. Our analysis shows, for the first time, effects of global warming on a honey bee pest and will help areas at risk to prepare adequately. In conclusion, this is a clear case for global warming promoting biological invasion of a pest species with severe potential to harm important pollinator species globally.     

Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens)

Here we explored the potential for host shift from honeybee, Apis mellifera, colonies to bumblebee, Bombus impatiens, colonies by the small hive beetle, a nest parasite/scavenger native to sub-Saharan Africa. We investigated small hive beetle host choice, bumblebee colony defence as well as individual defensive behaviour of honeybee and bumblebee workers. Our findings show that in its new range in North America, bumblebees are potential alternate hosts for the small hive beetle. We found that small hive beetles do invade bumblebee colonies and readily oviposit there. Honeybee colonies are not preferred over bumblebee colonies. But even though bumblebees lack a co-evolutionary history with the small hive beetle, they are able to defend their colonies against this nest intruder by removal of beetle eggs and larvae and stinging of the latter. Hence, the observed behavioural mechanisms must be part of a generalistic defence system suitable for defence against multiple attackers. Nevertheless, there are quantitative (worker force) and qualitative differences (hygienic behaviour) between A. mellifera and B. impatiens. Received 16 July 2007; revised 16 January 2008; accepted 17 January 2008.     

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.     

Uncovering the spatial pattern of invasion of the honeybee pest small hive beetle,Aethina tumida,in Italy

The fast tracking of invasion spatial patterns of alien species is crucial for the implementation of preventive and management strategies of those species. Recently, a honeybee pest, the small hive beetle Aethina tumida (hereafter SHB), has been reported in Italy, where it colonized more than 50 apiaries in an area of about 300 km². SHB is a nest parasite and scavenger of honeybee colonies native of Sub-Saharian Africa. Likely being helped by the globalization of apiculture, SHB underwent several invasions in the last twenty years, causing locally relevant economic impact. While many features of its biology have been addressed, an important knowledge gap concerns the spatial invasion dynamics in invaded areas. In this paper we coupled two spatial analysis techniques (geographic profiling and a density-based spatial clustering algorithm) to uncover the possible invasion pattern of SHB in Italy. We identified the port town of Gioia Tauro as the most likely point from which SHB may have spread and suggested the possible successive axes of diffusion. These putative diffusion paths suggest that the SHB spread in south Italy might have been due to a mix of natural dispersal between close apiaries and longer distance movement through faster, likely human-mediated, communication routes.     

Invasion pathway of the honeybee pest,small hive beetle,Aethina tumida (Coleoptera: Nitidulidae) in the Republic of Korea inferred by mitochondrial DNA sequence analysis

The small hive beetle (SHB), Aethina tumida, is native to the Sub-Saharan region of Africa, but it became invasive in many countries after its first introduction to the USA in 1996. The SHB is a destructive pest of the honey industry and can cause damage in apiaries due to feeding on the honey, pollen, honey bee brood and honey fermentation. SHB was recently found infesting honeybee colonies in the South-Eastern part of Korea, Miryang city in 2016. No inference of the origin or the pathway of the invasion into Korea has been made, so far. We analyzed partial cytochrome oxidase I gene of mitochondrial DNA to unveil the possible source of the invasive populations of SHB in South Korea. A Bayesian inference tree and median joining haplotype network revealed a strong relationship between South Korean and North American populations suggesting that the SHB in South Korea came from the USA. Low genetic variation among Korean populations suggests that the invasion might have occurred in a single event with small number of founders. In addition, a new global distributional map of SHB is provided.     

Identification of a bacterial pathogen associated with Porites white patch syndrome in the Western Indian Ocean

Porites white patch syndrome (PWPS) is a coral disease recently described in the Western Indian Ocean. This study aimed to isolate and identify potential pathogens associated with PWPS utilizing both culture and nonculture screening techniques and inoculation trials. A total of 14 bacterial strains (those dominant in disease lesions, absent or rare in healthy tissues and considered potential pathogens in a previous study) were cultured and used to experimentally inoculate otherwise healthy individuals in an attempt to fulfil Henle–Koch's postulates. However, only one (P180R), identified as closely related (99–100% sequence identity based on 1.4 kb 16S RNA sequence) to Vibrio tubiashii, elicited signs of disease in tank experiments. Following experimental infection (which resulted in a 90% infection rate), the pathogen was also successfully re‐isolated from the diseased tissues and re‐inoculated in healthy corals colonies, therefore fulfilling the final stages of Henle–Koch's postulates. Finally, we report that PWPS appears to be a temperature‐dependent disease, with significantly higher tissue loss (anova : d.f. = 2, F = 39.77, P < 0.01) occurring at 30 °C [1.45 ± 0.85 cm² per day (mean ± SE)] compared to ambient temperatures of 28 and 26 °C (0.73 ± 0.80 cm² per day (mean ± SE) and 0.51 ± 0.50 cm² per day (mean ± SE), respectively).     

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.     

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.     

Interspecific interactions change the outcome of sexual conflict over prehatching parental investment in the burying beetle Nicrophorus vespilloides

Sexual conflict arises when the optimal reproductive strategy differs for males and females. It is associated with every reproductive stage, yet few studies have considered how the outcome may be changed by interactions with other species. Here, we show that phoretic mites Poecilochirus carabi change the outcome of sexual conflict over the supply of prehatching parental investment in the burying beetle Nicrophorus vespilloides. Burying beetles require a small dead vertebrate for reproduction, which they prepare by shaving it, rolling up the flesh, and burying it. When pairs were given a medium‐sized mouse to prepare (13–16 g), mites changed how the costs of reproduction were divided between the sexes, with males then sustaining greater costs than females. We found no equivalent difference when pairs prepared larger or smaller carcasses. Thus, our experiment shows that the outcome of sexual conflict over prehatching parental investment is changed by interactions with other species during reproduction.