Besides humans, the common bed bug Cimex lectularius uses bats as hosts, but no such records were available from the Southern Caucasus. Here, we record the greater horseshoe bat (Rhinolophus ferrumequinum) and the lesser mouse-eared bat (Myotis blythii) as hosts of C. lectularius from two Georgian and one Armenian sites. A summary of all known published records of bat-associated populations of C. lectularius shows they are both scattered and restricted to the Palearctic only. Observations of C. lectularius from bat colonies in Georgia and Armenia were made in old buildings or ruins, like churches or monasteries, but not in caves, despite a specific search. This supports previous studies suggesting that 1) bat-associations of common bed bugs are very rare outside Central Europe and 2) almost never occur in caves. We discuss climatic conditions and host preferences as possible factors for these findings and the implications for the origin of the human bed bug interaction.

Bed bug, biogeography, ecology, ectoparasites, faunistics, host-parasite relationship, South Caucasus

The family Cimicidae (Heteroptera) constitutes a group of specialized haematophagous ectoparasitic insects. About two-thirds of the cimicid species are associated primarily with bats, which have been suggested to be the ancestral hosts of the family (Horváth 1913; but see Roth et al. 2019). The remaining species are associated with birds and only four cimicid species, among which the famous common bed bug Cimex lectularius Linnaeus, 1758, parasitize humans (Usinger 1966; Reinhardt and Siva-Jothy 2007). The Cimicidae contain about 110 species classified into 6 subfamilies and 24 genera (Henry 2017) and have a worldwide distribution. There are 17 species listed in Europe (Péricart 1996; Simov et al. 2006; Quetglas et al. 2012), including species of the Cimex pipistrelli species complex (for taxonomic discussion-see Roth et al. (2018)).

Both adults and nymphs stay on the body of their host only when feeding but otherwise hide nearby in the shelter of the host (Hase 1917). Outside shelters, however, several studies report cimicids – exclusively adults and mostly females – being attached to the host body (Loye, 1985; Heise, 1988; Rupp et al. 2004; Reinhardt and Jacobs 2006; Balvín et al. 2012a). Thus, if mated females can find a new location on their own, as such studies suggest, one can speculate that even if the transport itself is a passive transport by the bats, the attachment to the host body might potentially be an intentional behavior for dispersal.

In Europe, C. lectularius has been found in bat colonies (Usinger 1966; Roer 1969; Morkel 1999; Balvín et al. 2015) and occasionally also in bird nests (Günther and Niehus 1981; Vater 2015a,b; 2016). Association with bats almost exclusively occurs in bat reproduction roosts (e.g. Roer 1969) in human buildings (Balvín et al. 2015). Since their bat hosts hibernate in a different place (like caves), the bed bugs stay without their host species during the winter (e.g. Reinhardt 2012). So far, records of bat-associated C. lectularius, however, are rather rare outside central Europe (Balvín et al. 2015), but it is not clear whether this is due to a lack of search or a true distribution gap.

In the Southern Caucasus area, the common bed bug C. lectularius is well-known from human hosts/dwellings in Azerbaijan, Armenia, and Georgia (Dumas 1859, cited in Reinhardt 2014; Akramovskaya 1959; Gidayatov 1967; Zaytseva 1998; Aukema et al. 2013). But to the best of our knowledge, there are no records of cimicids related to bats as hosts in the Southern Caucasus. Here we undertook some field work and present the first records of C. lectularius associated with bats for the region. A detailed description of study places is given. Finally, we discuss some aspects of the ecology and distribution of C. lectularius associated with bats in Europe.

Material was sampled within the framework of the BMBF-funded Caucasus Barcode of Life (CaBOL) project (https://ggbc.eu/). The specimens were collected by hand, fixed in 96% ethanol, and later stored in a freezer under -22˚C for further DNA barcoding at the University Museum Bergen. Field work took place in May 20-23 (2022) in Armenia and from May 30 to June 2 (2022) in Georgia. In total, six and eight places were visited in Georgia and Armenia, respectively (Suppl. material 1). Seven of them were caves or tunnels, the other seven were churches or other human-made buildings.

All specimens were identified as Cimex lectularius. For all specimens, the pronotum was more than 2.5-3 times as wide as long (N=4: 3.30; 3.25; 2.80; 3.35) which excludes species from the Cimex pipistrelli-group. The ratio of length/width of the hind femur was >3.4 (N=4: 3.70; 3.50; 3.41; 3.60) which excludes Cimex emarginatus Simov, Ivanova and Schunger 2006. The ID based on morphological characters was confirmed by the COI DNA barcode, which is available at Genbank with the accession number OP897494.

Our field work revealed the presence of bat-associated Cimex lectularius at three out of 14 sites. We, therefore, suggest that the previous lack of bat-associated C. lectularius records in the Caucasus area was a result of low search efforts. Future fieldwork is, therefore, likely to yield more sites with bat-associated C. lectularius.

For setting our findings in a more general context, it is worth noting that while bat- and human associated populations of C. lectularius seem to be well able to interbreed (DeVries et al. 2020), but there is a relatively deep genetic divide between the two host lineages (Balvín et al. 2012b; Booth et al. 2015). This genetic isolation points towards a very low degree of interbreeding, suggesting that the Caucasus area was effectively colonized by both host lineages independently. If true, the independent colonization routes of the two lineages are the reason why the human-associated lineage occurs globally but not the bat-associated one. For example, no observations of bat-associated C. lectularius exist from North America, where the human-associated lineage is very abundant. In fact, published records of C. lectularius associated with bats come only from the following countries (see Figure 1), all within the Palearctic: Afghanistan (Povolný and Usinger 1966), Czech Republic (Povolný 1957), Finland (Poppius 1912), France (Usinger and Beaucournu 1967), Germany (e.g. Eichler 1937; Roer 1969; Morkel 1999; Reinhardt 2012), Hungary (Balvín et al. 2012b), Iran (Golestan province, N37.366°, E55.982°, 27 May 2006, A. Reiter and P. Benda leg.; assigned as bat-associated bed bug based on morphology by Balvín et al. 2012a; see also Roth et al. 2019), Iraq (Abul-Hab 1979; Lanza 1999), Kyrgyzstan (Rybin et al. 1989), Russia (Dauria steppe; Dubinin 1947), Serbia (Protić and Paunović 2006, misidentified as C. pipistrelli), Slovakia (Usinger 1966), Switzerland (Balvín et al. 2012b), Ukraine (Balvín et al. 2012a).

Figure 1. 

Records of Cimex lectularius associated with bats shown for different countries in the Palearctic.

Only two out of all these records, the ones from Afghanistan and the Domica Cave in Slovakia (Usinger 1966) concern findings in caves, i.e., in a natural, non-synanthropic habitats. Povolný and Usinger (1966) speculated that the former finding could represent an autochthonous bat-parasitizing population of the bed bug where humans acquired this parasite when they shared caves with bats as shelters (Horváth 1913; Usinger 1966). The status of Domica Cave as a bat roost in the past is difficult to assess. Nowadays, it is used as a summer roost for Miniopterus schreibersii and Rhinolophus euryale (Balvín, personal communication); neither species is known as a host for C. lectularius (Balvín et al. 2012b). It is unknown, if there ever were vital bed bug populations in that cave when it was used by Neolithic men.

The questions remaining are: 1) why is bat-associated C. lectularius rare in caves, and 2) why do we find a declining number of records from Central Europe to Southern Europe for both bat parasitic Cimex species (i.e. C. pipistrelli, C. lectularius) (Balvín et al. 2015)? A biased sampling effect cannot be excluded for many regions of the Palearctic. For Europe, however, exhaustive studies of bat roosts in Bulgarian caves have been conducted (Simov et al. 2006; Balvín et al. 2015).

Several factors, like bat host specificity of the common bed bug, habitat preferences due to climatic requirements of bed bugs, and in addition, climate preferences of the host species, are discussed as explanations for the European gradient (Simov et al. 2006; Balvín et al. 2015). For example, according to Simov (2006) the rarity of both Cimex spp. in bat caves might be because caves in Europe are too humid and too cold (see also Horacek 1983; Balvín et al. 2015). Human dwellings and bat boxes provide a warmer and drier alternative and more optimal summer roosts for many bat species and, thus, for their associated bed bugs as well. However, there are variations among local populations with different preferences for either caves or human dwellings (Balvín, personal communication).

Myotis spp. are the main bat host for the common bed bug (Balvín et al. 2015). The lack of stable and large colonies of Myotis spp. in southern Europe may mean the lack of a reservoir for stable C. lectularius populations (Balvín et al. 2015).

In summary, the biotic and abiotic factors discussed above might explain the lack of the common bed bug in caves in some parts of Europe. The question remains open as to why there are almost no records from caves in the entire Palearctic.

Our observations of bat-associated C. lectularius in Armenia and Georgia are the first records for the Caucasus. Moreover, all bugs were found in old churches, despite several caves being investigated. We found small but vital (reproductive) populations of C. lectularius connected to the following potential host species: Rhinolophus ferrumequinum and Myotis blythii. Since there were also some single individuals of M. emarginatus at Gremi Church, it cannot be excluded as another host species. But given the fact that the greater horseshoe bat forms a maternity colony of about 400 individuals there, it is very unlikely. Both Myotis spp. are known as hosts for C. lectularius (Balvín et al. 2012b; Balvín et al. 2015). Records of bed bugs in R. ferrumequinum colonies, however, are only known from mixed colonies with other bat species (Balvín et al. 2015). Further investigation at Gremi Church should reveal if the greater horseshoe bat is really the host of C. lectularius, which would be a new host species.

Entomological training plus a short additional field experience for unexperienced bat researchers may increase detection rates of cimicid bugs in bat colonies. More observational contributions from bat researchers, however, would certainly improve our knowledge about the distribution and ecology of bat associated bed bugs in Europe in general and in the Caucasus region in particular.

The project Caucasus Barcode of Life (CaBOL) – Assessing the Biodiversity of the Caucasus (ggbc.eu) on which this study is based was funded by the Federal Ministry of Education and Research under the grant number 01DK20014A. The responsibility for the content of this publication lies with the author.

We thank the members of Museum König Bonn for assistance during the field work in Armenia. Anna A. Namyatova (Zoological Institute St Petersburg) helped during the field trip in Georgia. We are very grateful to Nils Hein, the coordinator of the CaBOL project, for his engagement and management. Ondřej Balvín (Czech University of Life Sciences Prague Prague) shared his experience about bedbug-bat research and commented an earlier draft of the manuscript. Klaus Reinhardt (TU Dresden) and Astrid Pilz (Bergen) gave useful comments to improve the manuscript.