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Geographical map of the studied area. Shown are all sampled locations, with indication of those locations where we found infected bat flies. Arthrorhynchus eucampsipodae is reported only from Hungary, while A. nycteribiae is reported in both Hungary and Romania. Black dots represent locations where no Laboulbeniales fungi were found on the collected bat flies
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Background: Bat flies (Streblidae and Nycteribiidae) are among the most specialized families of the order Diptera. Members of these two related families have an obligate ectoparasitic lifestyle on bats, and they are known disease vectors for their hosts. However, bat flies have their own ectoparasites: fungi of the order Laboulbeniales. In Europe,...
Citations
... Gloeandromyces pageanus f. polymorphus has been reported on the flies Trichobius joblingi and on T. dugesioides associated with the bats C. perspicillata and Trachops cirrhosus (Spix, 1823), respectively (Haelewaters and Pfister 2019). The presence of the fungus near the bat fly gonopodium in our study may be explained by the fact that Laboulbeniales fungi are mainly transmitted during mating of bat flies (Haelewaters et al. 2018b), although other studies (Haelewaters et al. 2017a(Haelewaters et al. , 2017bWalker et al. 2018;Haelewaters and Pfister 2019) show that thalli of different fungal species or morphotypes may be restricted to a particular area of the host body (e.g., G. pageanus f. alarum, restricted to the base of the wings). ...
Hyperparasitism is defined as the interaction where one parasite is infected by another parasite. In bat flies (Streblidae and Nycteribiidae), both hyperparasites and microparasites (bacteria, viruses, fungi, and arthropods such as mites) have been documented. Fungi belonging to the order Laboulbeniales are microscopic parasites of a wide diversity of arthropod hosts. Three genera exclusively target bat flies: Arthrorhynchus, which parasitizes species within Nycteribiidae in the Eastern Hemisphere, while genus Gloeandromyces and Nycteromyces parasitize Streblidae in the Western Hemisphere. Among the hyperparasitic arthropods, mites of family Neothrombidiidae, particularly the monospecific genus Monunguis, are known to parasitize bat flies. Here we present the first records of the hyperparasites Monunguis streblida and Gloeandromyces pageanus f. polymorphus parasitizing Streblidae bat flies in Colombia and a summary of these hyperparasitic interactions in the Neotropics. We detected fungi and mites parasitizing bat flies that were collected in the Magdalena River Basin, Colombia, in field expeditions in 2018, 2022, and 2023. We identified 17 bat flies and two species of hyperparasites, specifically M. streblida and the fungi Gloeandromyces. Our search for reports of these interactions in the Neotropics revealed that seven species of Trichobius (Streblidae) are parasitized by M. streblida, whereas Paratrichobius longicrus (Streblidae) is parasitized by Gloeandromyces pageanus f. polymorphus. These interactions have been reported in 11 countries, but our records are the first of M. streblida and Laboulbeniales fungi parasitizing bat flies in Colombia. So far, a total of 14 species of fungi and one species of mite have been associated with 19 species of bat flies, which in turn, are linked to 15 species of Neotropical bats.
... Bat ies show a remarkable level of adaptation in morphology and behavior in accordance to their parasitic lifestyle to counteract the defense strategies of bats. There are around 570 bat y species worldwide from which 17 are present in Europe, with 10 species reported until now both from Romania, as well Bulgaria [9][10][11] . ...
... Any bat species hosting less than 5% of all individual occurrences was assigned the non-primary host status. Bat ies were characterized as monoxeonous, oligoxenous or polyxenous, according to the number of primary hosts 10,15 . We calculated the potential host-parasite connections (number of potential host species for each individual bat y species present at any given location, using the list of potential connections obtained from literature 9 ) and the realized host-parasite connections (number of host-parasite connections between any given bat y and its host species recorded at each sampling location). ...
Bat flies are the most abundant ectoparasites of bats, showing remarkable morphological adaptations to the parasitic habit, while the relationship with their hosts is characterized by a high level of specificity. By collecting bat flies from live hosts, our intention was to elucidate the seasonal differences in bat fly occurrence and to describe factors regulating the level of incipient host specificity. Our results indicate that the prevalence and the intensity of infestation is increasing from spring to autumn for most host species, with significant differences among different fly species. Males showed higher infestation levels than females in autumn, suggesting a non-random host choice by flies, targeting the most active host sex. Bat-bat fly host specificity shows seasonal changes and host choice of bat flies are affected by the seasonal differences in hosts’ behavior and ecology, the intensity of infestation and the species composition of the local host community. By choosing a non-primary bat host may be an adaptive choice for bat flies in the host’s mating period, thus increasing their dispersive ability in a high activity phase of their hosts.
... Nycteribiid bat flies, as ectoparasites, are parasitized by other organisms, including fungi, protozoa, and bacteria. These apterous bat flies have been reported to be infested by ectoparasitic fungi of the order Laboulbeniales (Blackwell, 1980;Haelewaters et al., 2017Haelewaters et al., , 2018Walker et al., 2018) and regarded as hyperparasites; and are hosts to the apicomplexan haemosporidian parasite, Polychromophilus, that causes bat malaria (Gardner and Molyneux, 1988;Obame-Nkoghe et al., 2016;Sándor et al., 2021). P. murinus is suspected to be transmitted by the nycteribiid bat fly, Nycteribia kolenatii (Gardner and Molyneux, 1988). ...
We investigated ectoparasite diversity, interspecific infestation rates and host preference in roosting fruit bats, Eidolon helvum, from Bowen University, Southwest Nigeria. Fur of captured E. helvum were sampled monthly for ectoparasites from January 2021 to June 2022. We examined a total of 231 E. helvum and observed a significant female to male adult sex ratio (0.22:1); with 53.9% ectoparasitic infestation rate. We identified and enumerated the ectoparasite; and subjected its Cytochrome c oxidase subunit I (COI) gene to phylogenetic analysis with other nycteribiids. COI gene sequences obtained formed a distinct clade with other C. greeffi sequences. We recovered a total of 319 (149 female and 170 male) ectoparasites and observed a balanced C. greeffi female to male adult sex ratio of 0.88:1. Ectoparasitic sex distribution had no association with host sex and season. Prevalence was significantly higher during the wet season, but not between sexes of E. helvum. The intensity of infestation, 3.7 ± 0.4 individuals per fruit bat, was significantly higher during the wet season with a bimodal seasonal distribution. The strongly male-biased host adult sex ratio had no significant influence on C. greeffi metapopulation adult sex ratio.
... Using the records of Szentivanyi et al. [21] as a starting point, we checked the literature on the host associations of European bat louse for new, overlooked, or misattributed records . In addition, we conducted a literature search using the keywords 'Nycteribiidae*', 'European bat flies*', 'host associations *', 'bats *', and 'Europe*' in Scopus and Google Scholar [7,51,52,[143][144][145][146][147][148][149][150][151][152][153][154]. Figures are redrawn and modified based on the original illustration by Theodor (1954) [155] (pp. ...
... For the host associations of European bat flies, we used information published by Szentivanyi et al. [21] and the recent literature [7,51,52,[143][144][145][146][147][148][149][150][151][152][153][154]. The terminology for the host specificity of particular bat fly species follows [156,157]. ...
Current taxonomical keys are essential for better biodiversity knowledge. Moreover, accurate identification of groups of organisms known to act as disease vectors is vital in today's world of change and the spread of zoonotic disease threats. This is especially relevant to bats and their parasites, given the events of recent years. The available keys of European Nycteribiidae (Diptera) are outdated and do not cover all the species currently known from Europe. Therefore, a summary key of 16 European species is provided in this paper. Based on published data from Europe, a total of 173 host-parasite interactions were observed between 16 European bat fly species and 31 host species (bats). The highest number of associations with different host species and the lowest specialization was observed in Penicillidia (P.) dufourii dufourii, followed by Nycteribia (N.) kolenatii, N. (N.) schmidlii and Phthiridium biarticulatum; most of the other species also had low specialization. Most species are oligoxenous, parasitizing on several families, and three species are stenoxenosus. Only one nycteribiid species, Basilia daganiae, was linked with only one host (Pipistrellus kuhlii). Myotis myotis has 12 associations with different bat fly species, followed by Plecotus auritus and Myotis daubentonii with 12 associations. A relatively high number of bat species were associated with only one bat fly species. In addition, we performed a bipartite analysis complemented by network indices and host specificity at the species and whole network levels, yielding new information in terms of ecology and the host-parasite relationships related to these groups of potential vectors (Nycteribiidae) and sources of zoonoses (bats). The parasite-host network composed of 16 nycteribiid species and 31 bat host species was characterized by a low network level specialization, low modularity, and low nestedness. Our findings also suggest a high probability of associated Nycteribiidae in bat taxa with a similar roosting ecology and phylogenetic relationship.
... Termed a risky lifestyle, hyperparasitism may have arisen independently more than once [44]. The phenomenon of microbes parasitizing parasites of other organisms has been reported for bacteria, fungi, haemosporidian endoparasites and fungi [44][45][46][47]. [59] The table summarizes bat ectoparasite virome studies conducted globally with an indication of the general area (continent/sub-continent), ectoparasite family or species, method of virus isolation or identification, and inferences made on ectoparasite role in virus transmission. ...
Humans continue to encroach on the habitats of wild animals, potentially bringing different species into contact that would not typically encounter each other under natural circumstances, and forcing them into stressful, suboptimal conditions. Stressors from unsustainable human land use changes are suspected to dramatically exacerbate the probability of zoonotic spillover of pathogens from their natural reservoir hosts to humans, both by increasing viral load (and shedding) and the interface between wildlife with livestock, pets and humans. Given their known role as reservoir hosts, bats continue to be investigated for their possible role as the origins of many viral outbreaks. However, the participation of bat-associated ectoparasites in the spread of potential pathogens requires further work to establish. Here, we conducted a comprehensive review of viruses, viral genes and other viral sequences obtained from bat ectoparasites from studies over the last four decades. This review summarizes research findings of the seven virus families in which these studies have been performed, including Paramyxoviridae, Reoviridae, Flaviviridae, Peribunyaviridae, Nairoviridae, Rhabdoviridae and Filoviridae. We highlight that bat ectoparasites, including dipterans and ticks, are often found to have medically important viruses and may have a role in the maintenance of these pathogens within bat populations.
... The fourth dataset lists the parasitic bat flies and their Laboulbeniales fungal hyperparasites associated with cave bats. Data were collected from several sources, including our fieldwork data 36 , Haelewaters et al. 44 , and de Groot et al. 45 . Bat fly taxonomy followed Dick and Graciolli 46 and Graciolli and Dick 47 and fungal taxonomy followed Index Fungorum 48 . ...
Understanding biodiversity patterns as well as drivers of population declines, and range losses provides crucial baselines for monitoring and conservation. However, the information needed to evaluate such trends remains unstandardised and sparsely available for many taxonomic groups and habitats, including the cave-dwelling bats and cave ecosystems. We developed the DarkCideS 1.0 (https://darkcides.org/), a global database of bat caves and species synthesised from publicly available information and datasets. The DarkCideS 1.0 is by far the largest database for cave-dwelling bats, which contains information for geographical location, ecological status, species traits, and parasites and hyperparasites for 679 bat species are known to occur in caves or use caves in part of their life histories. The database currently contains 6746 georeferenced occurrences for 402 cave-dwelling bat species from 2002 cave sites in 46 countries and 12 terrestrial biomes. The database has been developed to be collaborative and open-access, allowing continuous data-sharing among the community of bat researchers and conservation biologists to advance bat research and comparative monitoring and prioritisation for conservation.
... The first list of Romanian bat flies was published more than 50 years ago (Decu-Burghele 1962), followed by several papers usually treating particular species (e.g., Decu-Burghele 1963; or regions (e.g., Burghele-Bălăcescu 1966;Gheorghiu 2006). Recently, several studies targeting bats and their parasites were initiated, with a high number of bat flies collected and analyzed (Hornok et al. 2016(Hornok et al. , 2017Haelewaters et al. 2017;Hornok et al. 2019;Sándor et al. 2019;Péter et al. 2022). ...
... This annotated checklist is based on the published literature up to 2021 and field surveys from 2017 to 2020. Altogether, we found 20 articles containing original data on bat flies from Romania (Kolenati 1857b;Thalhammer 1899;Bokor 1921;Dudich 1925;Decu-Burghele 1962, 1963Dumitrescu et al. 1965;Burghele-Bălăcescu 1966;Negrea et al. 1967;Rădulescu & Lustun 1967;Theodor 1967;Blackwell 1980;Gheorghiu 2006;Willemsen & Thomassen 2009;Postawa & Nagy 2016;Haelewaters et al. 2017;Sándor et al. 2018;McKee et al. 2019;Sándor et al. 2021), covering more than 170 years in terms of collection dates. In the period 2017-2020, we collected 2975 bat flies (belonging to ten species) from 1196 bats (22 host species). ...
... Published records. Peștera Liliecilor de la Gura Dobrogei (Burghele-Bălăcescu 1966), host unknown; Avenul Betfia, Somova (Haelewaters et al. 2017;Sándor et al. 2018;McKee et al. 2019;Sándor et al. 2021), host Miniopterus schreibersii (Kuhl). Canaraua Fetii, Peștera Tunel de la Hagieni, Somova (Haelewaters et al. 2017;Sándor et al. 2018;McKee et al. 2019) host My. bechsteinii. ...
Bat flies (Diptera: Hippoboscoidea: Nycteribiidae, Streblidae) are obligate, blood-feeding, highly specialized ectoparasites of bats (Chiroptera). Of the 17 nycteribiid species present in Europe, 11 have been recorded in Romania. Here, we present a checklist with all the previously published data and new records from recent years, for a total of 2218 records of bat-bat fly associations. Host-parasite associations are updated for Basilia italica Theodor, B. nana Theodor, B. nattererii (Kolenati), Nycteribia kolenatii Theodor & Moscona, N. latreillii (Leach), N. pedicularia Latreille, N. schmidlii Schiner, N. vexata Westwood, Penicillidia conspicua Speiser, Pe. dufourii (Westwood) and Phthiridium biarticulatum Hermann.
... Several studies on multitrophic relationships have targeted hyperparasites in biological control strategies (Verkerk et al., 1998;Tougeron and Tena, 2019). A recently resurfaced example of hyperparasitism is the tritrophic association found among bats (Mammalia: Chiroptera), their ectoparasitic bat flies (Diptera: Hippoboscidae: Nycteribiidae and Streblidae), and fungal biotrophic parasites of the dipterans (Ascomycota: Laboulbeniomycetes) (Haelewaters et al., 2017(Haelewaters et al., , 2021bde Groot et al., 2020). ...
... The vast majority of Laboulbeniales species, around 80% percent of the currently known 2,325 species, infect insects from the order Coleoptera, whereas only some 10% are found on representatives of the order Diptera (Weir and Hammond, 1997). Currently two described species of Arthrorhynchus are known to be associated with nycteribiid flies in Europe (Haelewaters et al., 2017), and at least one of these taxa represents a species complex . In recent years, the scientific interest in Laboulbeniales fungi of bat flies has increased, as this system represents a model to study hyperparasitic relationships. ...
... Haelewaters et al. (2021b) called for global collaborations to build non-biased datasets resulting from multitrophic fieldwork sensu Walker et al. (2018). Such datasets may be essential in answering community ecological questions (e.g., whether habitat destruction affects parasitism at multiple levels) and in studying disease transmission through bat flies (Haelewaters et al., 2017;de Groot et al., 2020). ...
The tritrophic association of bats, bat flies, and Laboulbeniales microfungi is a remarkably understudied system that may reveal patterns applicable to community ecology theory of (hyper)parasites. Laboulbeniales are biotrophic microfungi, exclusively associated with arthropods, with several species that are specialized on bat flies, which themselves are permanent ectoparasites of bats. Several hypotheses were tested on biotic and abiotic traits that may influence the presence and prevalence of hyperparasitic Laboulbeniales fungi on bat flies, based on southeastern European data. We found a wide distribution of fungal infection on bat flies, with underground-dwelling bats hosting more Laboulbeniales-infected flies compared to crevice-dwelling species. Bat host behavior, sociality, roost selection (underground versus crevice), bat fly sex, and season all have significant effects on the prevalence of fungal infection. Laboulbeniales infections are more common on bat flies that are infecting bat species with dense and long-lasting colonies (Miniopterus schreibersii, Myotis myotis, Myotis blythii), which roost primarily in underground sites. Inside these sites, elevated temperature and humidity may enhance the development and transmission of Laboulbeniales fungi. Sexual differences in bat hosts’ behavior also have an effect on fungal infection risk, with densely roosting female bat hosts harboring more Laboulbeniales-infected bat flies.
... A parasite itself can be infected with another parasite, which defines the latter as a hyperparasite 2 . Understanding parasitism, especially hyperparasitism, requires a complex multidisciplinary approach involving ecology, evolution and behaviour of the three participants in the interaction [2][3][4][5] . ...
Laboulbeniales are a highly specialized group of fungi living only on arthropods. They have high host specificity and spend their entire life-cycle on an arthropod host. Taxonomic characters of Laboulbeniales are based on the architecture of the cells of the parenchymal thallus, i.e. the visible part of the fungus outside the host. The extent of the fungus spreading inside the host—the haustorium—remains largely unknown. The attachment to the arthropod host is fundamental to understand the fungus-animal interaction, but how this truly occurs is unclear. Recent evidences question the strictly parasitic life-style of Laboulbeniales. We used micro-computed tomography (µCT) and 3D reconstructions to visualize, for the first time, the complete structure of Laboulbeniales species in situ on their hosts. We compared the haustoriate species, Arthrorhynchus nycteribiae on an insect host to the non-haustoriate species, Rickia gigas on a millipede host. Our results confirm that some Laboulbeniales species are ectoparasitic and have a haustorial structure that penetrates the host’s cuticle, while others are ectobionts and are only firmly attached to the host’s cuticle without penetrating it. The presence and the morphology of the haustorium are important traits for Laboulbeniales evolution, and key factors for future understanding of host dependence and specificity.
... The fourth dataset lists the parasitic bat flies and their Laboulbeniales fungal hyperparasites associated with cave bats. Data were collected from several sources, including our own fieldwork 36 , Haelewaters et al. 40 , and de Groot et al. 41 . Bat fly taxonomy followed Dick and Graciolli 42 and Graciolli and Dick 43 and fungal taxonomy followed Index Fungorum 44 . ...
Understanding biodiversity patterns as well as drivers of population declines, and range losses provides crucial baselines for monitoring and conservation. However, the information needed to evaluate such trends remains unstandardised and sparsely available for many taxonomic groups and habitats, including the cave-dwelling bats and cave ecosystems. Here, we present the DarkCideS 1.0 , a global database of bat caves and bat species based on curated data from the literature, personal collections, and existing datasets. The database contains information for geographical distribution, ecological status, species traits, and parasites and hyperparasites for 679 bat species known to occur in caves or use caves in their life-histories. The database contains 6746 georeferenced occurrences for 402 cave-dwelling bat species from 2002 cave sites in 46 countries and 12 terrestrial biomes. The database has been developed to be a collaborative, open-access, and user-friendly platform, allowing continuous data-sharing among the community of bat researchers and conservation biologists. The database has a range of potential applications in bat research and enables comparative monitoring and prioritisation for conservation.
