The multi-species associations of insects (symbiocenosis) in honey bee hives currently include more than 15 orders of Insecta. We present the results of studying the inquilines of bee hives in the south of Western Siberia. In the honeybee hives of this region 37 insect species from 8 orders (Dermaptera, Thysanoptera, Psocoptera, Hemiptera, Coleoptera, Hymenoptera, Lepidoptera, Diptera) were identified. Inquiline insects were observed in 77% of hives in 81.5% of the studied apiaries. Coleoptera prevailed among the orders, accounting for 94% of observations. The overall eudominant was Cryptophagus scanicus (Linnaeus, 1758) (87.8%); the subdominants were Dermestes lardarius Linnaeus, 1758 and Contacyphon variabilis (Thunberg, 1787). The smallest number of insect species can be attributed to specific groups. These are C. scanicus, a detritophage that primarily feeds on mold fungi hyphae, but can also consume bee supplies; and Galleria melonella (Linnaeus, 1758), a widespread pest of bee colonies, that feeds on bee bread, honey, wax and bee brood. The facultative group includes detritophages, pollen- and honey-feeding species, that find suitable conditions for feeding and developing in beehives (Vespidae, Formicidae, etc.). Representatives of accidental group were the most diverse in species composition and type of nutrition but they were always individually found in hives. In total, 42 species of insects are currently recorded in the beehives of Western Siberia.

Bee hives, beekeeping, Coleoptera, Galleria melonella, honey bee hives, Insecta

The honey bee nest is an apiophilic symbiocenosis of the nidicolous (nest) type (Sidorov 1968). A honeybee hive can be considered an artificial nidicolous ecotope – a community habitat with sufficient ventilation and a relatively stable microclimate that provide favorable conditions for symbionts – consortium members (Bakalova 2011a).

Arthropods are an integral part of bee hive biocenosis. Mites and insects are the main symbionts of bees, predominant in quantity and taxonomic diversity (Stolbova 2022).

Insects (Insecta) show the most diversity in apiophilic symbiocenoses, to date representatives of the Collembola and 14 orders insects have been noted: Zygentoma, Blattodea, Dermaptera, Psocodea, Thysanoptera, Heteroptera, Coleoptera, Hymenoptera, Neuroptera, Raphidiodea, Lepidoptera, Mecoptera, Diptera, Siphonaptera (Orösi Pal 1939; Sidorov 1968; Banaszak 1980; Bakalova 2011a; Semmar et al. 2014). The total number of insects found in honeybee hives amounts to several hundred species (Bakalova 2011a).

The most numerous insect symbionts of bees are Coleoptera (Sidorov 1968). According to the latest data, the list of beetles in honeybee hives includes 155 species from 30 families (Bakalova 2011a).

Among insects, there are both specific species whose entire life cycle is tied to bees, and numerous facultative species that visit hives periodically, or enter them accidentally, for example, in search of shelter for wintering.

A range of insect species is serious pests of beekeeping, primarily the greater wax moth Galleria mellonella (Linnaeus, 1758) and the lesser wax moth Achroea grisella (Fabricius, 1794). Some Coleoptera are also serious pests, in particular, Aethina tumida Murray, 1867, which has been actively settling in different countries in recent years (Neumann et al. 2016).

A number of researchers believe that wasps occupy the first place among the pests of honey bees from the insect class, in terms of damage caused. To date, there are 26 species and subspecies of honey bee pest wasps from 6 genera and 2 families (Pusceddu et al. 2017; Konovalova 2018). There are over 50 species of Diptera associated with bees, most of them are parasitoids (Zimina 1973; Bakalova 2011a).

In addition to the direct harm caused to bees, many insects can be carriers of fungal spores and viruses that cause diseases of bees, such as nosematosis, ascospherosis, etc. Beetles transfer mold spores and Nosema apis (Zander, 1909) microsporidia from the bottom of the hive to the honeycomb of the brood nest or from one hive another. It was found that single adult individuals of Tribolium madens (Charpentier, 1825) and Dermestes lardarius Linnaeus, 1758 can carry about 150 and 285 thousand spores of Ascosphaera apis (Maasen ex Claussen) Olive & Spiltoir, 1955 – the causative agent of ascospherosis of bees on the surface of their bodies (Measures to control beetles 1998).

However, most of the insects found in hives are commensals, which often not only do not harm beekeeping but on the contrary, are useful. First of all, these are detritophages, which dispose of garbage, mold fungi and dead bees from the bottom of hives. These include beetles, earwigs, cockroaches. These species feed on the waste of bee colonies (wax crumbs, contaminated bee bread, feces and corpses of bees) and thus, contribute to the cleaning of the honey bee nest.

No less important for bee symbiocenosis are predatory insect species that regulate the number of other arthropods in the hive. This group includes beetles (Carabidae, Staphilinidae, Coccinellidae, etc.), Hymenoptera (Vespidae, Formicidae), Raphidioptera, Chrysopidae, etc. (Bakalova 2011a). Permanent predatory species of hive symbionts, as a rule, are mutualists in relation to bees but facultative species ones can be harmful (Measures to control beetles 1998).

There are quite a large number of papers on bee symbionts, however, most of them cover individual practically significant species, such as Varroa destructor ticks Anderson & Trueman, 2000, wax moth, small hive beetle and other bee parasites and pests. The most complete reports on the entomofauna of bee hives were obtained quite a long time ago, and mainly cover Europe (Orösi Pal 1939; Banaszak 1980). These papers describe the composition of symbionts give general data on their ecology.

A number of works are available on the European part of Russia and the Caucasus (Sidorov 1968; Atakishiev 1969; Pushkin 2009; Bakalova 2011a). At the same time, in all the above works, the emphasis was placed either on individual groups of symbionts (according to the degree of harmfulness to bees), or on specific conditions of detention (bee-trees, wild hive).

In Siberia, there are papers on specific groups of symbiont insects (Coleoptera, earwigs) (Zbanatsky 1997b; Domatsky and Domatskaya 2020). At the same time, considering the symbiocenosis of the nidicolous type, all members of which are important for its full functioning, it is necessary to study all bee symbionts in the complex.

Earlier, we studied in detail the composition of the acarofauna of honey bee hives in Western Siberia (Stolbova 2022). This paper considers entomofauna.

The topic was studied in 2020–2022 in the south of Western Siberia, within the southern taiga and forest-steppe zones. The short summer period in this region is characterized by high temperatures, the winter period is long and severe (5–6 months), with frequent frosts. The main breed of bees in the region is Apis m. mellifera Linnaeus, 1758, but beekeepers also contain other breeds, such as the Apis m. carpathica Avetisyan, Gubin & Davidenco, 1966, Apis m. carnica Pollmann, 1879, and Apis m. buckfast, thus most of the bees in Western Siberia are mixed (Pashayan and Endovitsky 2018).

A total of 193 bee colonies from 27 apiaries from 20 settlements in the south of the Sverdlovsk Oblast, Tyumen Oblast and Altai Krai were studied. Collection from the south of the Tyumen Oblast prevailed. A detailed description of the collection points is to be found in (Suppl. material 1).

For the study, dead bees, wax and bee bread crumbs, and waste from the bottom of hives were collected in paper bags, labelled and delivered to the laboratory. Part of the material was selected and provided to the laboratory by apiaries owners.

To study the qualitative and quantitative composition of the bee hive fauna, the same amount of dead bees was taken from the selected or received material in the laboratory, the quantity was a standard completely full Falcon-type test tube (volume 50 ml). The sample was filled with water and kept for 1–2 hours, periodically turning the tube over to mix the contents. After that, the sample was carefully examined under a stereomicroscope against a dark background.

Some of the samples were pre-treated in Berlese funnel for 2 weeks until the substrate was completely dry. After that, the dry residue was examined under a stereomicroscope.

Thysanoptera, Psocoptera, Hemiptera, Hymenoptera (Formicidae, Parasitica), Diptera insects and all insect larvae were fixed in 70% alcohol, the rest were placed on entomological mattresses. Coleoptera and Hemiptera were subsequently mounted on entomological plates. Psocoptera were mounted on slides using Hoyer’s medium. Taxonomic identification of symbionts was made using identification guides, scientific articles and Internet resources (Bey-Bienko 1965; Ler 1992; Lyubarsky 2002; Ellis et al. 2013; Opit G et al. 2022).

Statistical data processing was carried out in the Microsoft Excel 2016 program. In this paper, the following terms are used: abundance – the number of insects per infected sample (min–max, average, ex.); occurrence – the number of samples (bee colonies) with insects, as a percentage of the number of samples studied; dominance index – the number of individuals of this species to the total number of individuals of all detected species (%).

A total of 37 insect species were identified (Table 1). Some of the insects were identified only to genus or family, since many specimens lacked diagnostic features. Identification of larvae was often especially difficult.

Nine insect species were found in bee hives for the first time: Cryptophagus hauseri, Sciodrepoides watsoni, Phyllobius contemptus, Epuraea biguttata, E. boreella, Brachypterus fulvipes, Litargus connexus (Coleoptera), Scolopostethus pictus and Rhyparochromus pini (Heteroptera).

In addition to these species, Forficula tomis, Formica rufibarbis and Liposcelis bostrychophila were recorded in bee brood nests in Western Siberia for the first time.

Other insect species were regularly observed in honey bee hives, including in Western Siberia.

In numbers of species, the Coleoptera predominated, which accounted for half (18) of all identified insect species. Hymenoptera were also quite numerous, at the same time the particular spices of Parasitica representatives were not identified. The remaining orders were represented by just one or two species.

Symbiont insects were observed in 81.5% of the studied apiaries (Table 2). The occurrence in the studied bee hives was 77%.

Both in terms of occurrence, and especially in number, representatives of Coleoptera prevailed among the orders, which accounted for 94% of all insects detected.

The absolute dominant species was Cryptophagus scanicus, which, the preimaginal stages included, accounted for 93.2% of all beetles and 87.8% of all insects.

Two other species of Coleoptera, Dermestes lardarius and Contacyphon variabilis, also had a fairly high number: D. lardarius, larval stages included accounted for 2.1% of all insects, and the second species took 2.8%. It is characteristic that in the most numerous symbionts – C. scanicus and D. lardarius, larval stages prevailed in the studied hives (88.4% and 88.5%, respectively).

Vespula germanica wasps, Parasitica and a greater wax moth also had a relatively high occurrence and abundance. The rest of the insect representatives were observed singly.

The occurrence of symbionts in different apiaries varied. Of the 37 insect species found, less than half (16) were recorded in two or more apiaries (44.4%).

The occurrence of symbionts among the studied bee colonies was not very high (Table 2), with the exception of C. scanicus, all species had an occurrence below 20%. However, the occurrence in the studied apiaries was significantly higher, while in the dominant species it almost did not change. This shows that the dominant species had a consistently stable high occurrence both in different apiaries and in bee colonies in the same apiary, while other insect species associated with bees were also regularly found in different apiaries of the studied region, although they had a lower number.

The insects found in hives can be divided into several ecological groups that play different roles in hives (Fig. 1).

Figure 1. 

Proportion of ecological groups of insects by abundance (outer circle) and number of species (inner circle): 1 – specific species, 2a, 2b – facultative species (a – Detritophages; b – species feeding on pollen and honey), 3 – accidental species.

Earlier, one paper on beetles in hives of Western Siberia in the region lists 22 species of Coleoptera – symbionts of bees (Zbanatsky 1997a). Our research complements the list of 20 species of Coleoptera and other insects. Thus, at the moment, 42 species of insects have been recorded in bee hives in Western Siberia.

At the turn of the 20^th and 21^st centuries, the same species prevailed in the bee hives of Western Siberia – the specific commensal C. scanicus, the marsh beetles C. variabilis were numerous. These results match the results of our study. Facultative and accidental species were diverse but not numerous. At the same time, in our study did not occure Tribolium madens, indicated as numerous in previosly study, which can be a serious pest of hives (Zbanatsky 1997a).

The species composition and structure of bee symbionts in Western Siberia are very similar to the symbiocenoses of hives in the regions of the European part of Russia and other countries (Kazakhstan, Poland) (Rolnik and Szmidt 1959; Banaszak 1980; Semmar et al. 2014; Skulachev 2017). In most studies, a few specific species had the greatest number and occurrence. Cryptophagus scanicus is a typical commensal of bees, which dominates in number and occurrence in many regions. Such facultative species as ants, earwigs and the German wasp are regularly and in large numbers recorded in hives of Russia, Europe and other countries (links). The latter, which has become cosmopolitan thanks to human activities, is noted in most countries of the world, is numerous in hives and is considered one of the most dangerous pests of beekeeping.

The study of the fauna of insects living in honeybee hives should be continued, paying special attention to the role of marsh beetles and Parasitica in the structure of the symbiocenosis of bee colonies.

The authors expresses deep gratitude for help in identifying some doubtful species of insects to A.G. Kirejtshuk (Nitidulidae, Kateretidae), A.V. Kovalev (Latridiidae), A.A. Legalov (Curculionidae), G.Yu. Lyubarsky (Cryptophagidae), S.A. Ivanov (Heteroptera), A.S. Sazhnev (Scirtidae). Authors also wish to thank Stephen J. Martin (University of Salford, Manchester, United Kingdom) and Michał Woyciechowski (Jagiellonian University, Kraków, Poland) for valuable comments when reviewing the article. The paper has been prepared with the financial support from the Ministry of Education and Science within the framework of the project 121042000066-6 “Study and analysis of the epizootic state of diseases of invasive etiology of agricultural and unproductive animals, bees and birds, changes in the species composition and bioecological patterns of the development cycle of parasites in conditions of displacement of their habitats”.