Parasites of parasites of bats: Laboulbeniales (Fungi: Ascomycota) on bat flies (Diptera: Nycteribiidae) in central Europe.
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ABSTRACT: 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, members of the Nycteribiidae are parasitized by four species belonging to the genus Arthrorhynchus. We carried out a systematic survey of the distribution and fungus-bat fly associations of the genus in central Europe (Hungary, Romania).We encountered the bat fly Nycteribia pedicularia and the fungus Arthrorhynchus eucampsipodae as new country records for Hungary. The following bat-bat fly associations are for the first time reported: Nycteribia kolenatii on Miniopterus schreibersii, Myotis blythii, Myotis capaccinii and Rhinolophus ferrumequinum; Penicillidia conspicua on Myotis daubentonii; and Phthiridium biarticulatum on Myotis capaccinii. Laboulbeniales infections were found on 45 of 1,494 screened bat flies (3.0%). We report two fungal species: Arthrorhynchus eucampsipodae on Nycteribia schmidlii, and A. nycteribiae on N. schmidlii, Penicillidia conspicua, and P. dufourii. Penicillidia conspicua was infected with Laboulbeniales most frequently (25%, n?=?152), followed by N. schmidlii (3.1%, n?=?159) and P. dufourii (2.0%, n?=?102). Laboulbeniales seem to prefer female bat fly hosts to males. We think this might be due to a combination of factors: female bat flies have a longer life span, while during pregnancy female bat flies are significantly larger than males and accumulate an excess of fat reserves. Finally, ribosomal DNA sequences for A. nycteribiae are presented.We screened ectoparasitic bat flies from Hungary and Romania for the presence of ectoparasitic Laboulbeniales fungi. Arthrorhynchus eucampsipodae and A. nycteribiae were found on three species of bat flies. This study extends geographical and host ranges of both bat flies and Laboulbeniales fungi. The sequence data generated in this work contribute to molecular phylogenetic studies of the order Laboulbeniales. Our survey shows a complex network of bats, bat flies and Laboulbeniales fungi, of which the hyperparasitic fungi are rare and species-poor. Their host insects, on the other hand, are relatively abundant and diverse.
<h4>Background</h4>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, members of the Nycteribiidae are parasitized by four species belonging to the genus Arthrorhynchus. We carried out a systematic survey of the d ...[more]
Project description:BackgroundBat flies (Diptera: Nycteribiidae and Streblidae) are obligate, blood-sucking ectoparasites of bats with specialized morphology, life-cycle and ecology. Bat flies are occasionally infected by different species of Laboulbeniales (Fungi: Ascomycota), microscopic fungal ectoparasites belonging to three genera: Arthrorynchus spp. are restricted to the Eastern Hemisphere, while species of Gloeandromyces and Nycteromyces occur on Neotropical bat flies. Little is known about the distribution and host specificity of Arthrorynchus spp. on bat flies. In this study, we focused on sampling bat flies from the cave-dwelling bat species Miniopterus schreibersii. Bat and ectoparasite collection took place in Albania, Croatia, Hungary, Italy, Portugal, Slovakia, Spain and Switzerland. Flies were inspected for Laboulbeniales infections.ResultsSix hundred sixty seven bat flies of five species were collected: Nycteribia latreillii, N. pedicularia, N. schmidlii, Penicillidia conspicua, and P. dufourii. Laboulbeniales infection was observed on 60 specimens (prevalence = 9%). Two Laboulbeniales species, Arthrorhynchus eucampsipodae and A. nycteribiae, were present on three bat fly species. All observations of A. eucampsipodae were on N. schmidlii, and A. nycteribiae was present on P. conspicua and P dufourii. Arthrorhynchus eucampsipodae is, for the first time, reported from Slovakia and Spain. Arthrorhynchus nycteribiae represents a new country record for Portugal and Slovakia. There were no significant differences among infection rates in different countries. Females of N. schmidlii showed a higher infection rate than males with an observable trend (P = 0.0502). No sex differences in infection rate for P. conspicua and P. dufourii were detected. Finally, thallus density was significantly lower in N. schmidlii compared to P. conspicua and P. dufourii.ConclusionsWith this study, we contribute to the knowledge of the geographical distribution and host specificity of Laboulbeniales fungi associated with ectoparasitic bat flies within Europe. We discuss parasite prevalence and host specificity in the light of our findings and the available literature. Penicillidia conspicua is unambiguously the main host species for A. nycteribiae based on our and previous findings. Differences in parasite intensity and sex-biased infections of the fungi are possible depending on the species.
Project description:The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere (Arthrorhynchus) and twice in the Western Hemisphere (Gloeandromyces, Nycteromyces). We hypothesize that the genera Arthrorhynchus and Nycteromyces evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus Gloeandromyces by considering the LSU rDNA region. Phenotypic plasticity and position-induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, G. pageanus and G. streblae, show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.
Project description:Previous and ongoing studies have incriminated bats as reservoirs of several emerging and re-emerging zoonoses. Most of these studies, however, have focused on viral agents and neglected important bacterial pathogens. To date, there has been no report investigating the prevalence of Bartonella spp. in bats and bat flies from Nigeria, despite the fact that bats are used as food and for cultural ritual purposes by some ethnic groups in Nigeria. To elucidate the role of bats as reservoirs of bartonellae, we screened by molecular methods 148 bats and 34 bat flies, Diptera:Hippoboscoidea:Nycteribiidae (Cyclopodia greeffi) from Nigeria for Bartonella spp. Overall, Bartonella spp. DNA was detected in 76 out of 148 (51.4%) bat blood samples tested and 10 out of 24 (41.7%) bat flies tested by qPCR targeting the 16S-23S internal transcribed spacer (ITS) locus. Bartonella was isolated from 23 of 148 (15.5%) bat blood samples, and the isolates were genetically characterized. Prevalence of Bartonella spp. culture-positive samples ranged from 0% to 45.5% among five bat species. Micropterus spp. bats had a significantly higher relative risk of 3.45 for being culture positive compared to Eidolon helvum, Epomophorus spp., Rhinolophus spp., and Chaerephon nigeriae. Bartonella spp. detected in this study fall into three distinct clusters along with other Bartonella spp. isolated from bats and bat flies from Kenya and Ghana, respectively. The isolation of Bartonella spp. in 10.0-45.5% of four out of five bat species screened in this study indicates a widespread infection in bat population in Nigeria. Further investigation is warranted to determine the role of these bacteria as a cause of human and animal diseases in Nigeria.
Project description:Bat flies are a diverse clade of obligate ectoparasites on bats. Like most blood-feeding insects, they harbor endosymbiotic prokaryotes, but the origins and nature of these symbioses are still poorly understood. To expand the knowledge of bacterial associates in bat flies, the diversity and evolution of the dominant endosymbionts in six of eight nominal subfamilies of bat flies (Streblidae and Nycteribiidae) were studied. Furthermore, the localization of endosymbionts and their transmission across developmental stages within the family Streblidae were explored. The results show diverse microbial associates in bat flies, with at least four ancestral invasions of distantly related microbial lineages throughout bat fly evolution. Phylogenetic relationships support the presence of at least two novel symbiont lineages (here clades B and D), and extend the geographic and taxonomic range of a previously documented lineage ("Candidatus Aschnera chinzeii"; here clade A). Although these lineages show reciprocally monophyletic clusters with several bat fly host clades, their phylogenetic relationships generally do not reflect current bat fly taxonomy or phylogeny. However, within some endosymbiont clades, congruent patterns of symbiont-host divergence are apparent. Other sequences identified in this study fall into the widely distributed, highly invasive, insect-associated Arsenophonus lineage and may be the result of symbiont replacements and/or transient infections (here clade C). Vertical transmission of endosymbionts of clades B and D is supported by fluorescent signal (fluorescent in situ hybridization [FISH]) and microbial DNA detection across developmental stages. The fluorescent bacterial signal is consistently localized within structures resembling bacteriomes, although their anatomical position differs by host fly clade. In summary, the results suggest an obligate host-endosymbiont relationship for three of the four known symbiont clades associated with bat flies (clades A, B, and D).
Project description:Parasitism is one of the most diverse and abundant modes of life, and of great ecological and evolutionary importance. Notwithstanding, large groups of parasites remain relatively understudied. One particularly unique form of parasitism is hyperparasitism, where a parasite is parasitized itself. Bats (Chiroptera) may be parasitized by bat flies (Diptera: Hippoboscoidea), obligate blood-sucking parasites, which in turn may be parasitized by hyperparasitic fungi, Laboulbeniales (Ascomycota: Laboulbeniomycetes). In this study, we present the global tritrophic associations among species within these groups and analyze their host specificity patterns. Bats, bat flies, and Laboulbeniales fungi are shown to form complex networks, and sixteen new associations are revealed. Bat flies are highly host-specific compared to Laboulbeniales. We discuss possible future avenues of study with regard to the dispersal of the fungi, abiotic factors influencing the parasite prevalence, and ecomorphology of the bat fly parasites.
Project description:BACKGROUND:We present information on Nycteribiidae flies parasitizing the bat families Pteropodidae, Miniopteridae and Vespertilionidae from the Malagasy Region, contributing insight into their diversity and host preference. RESULTS:Our phylogenetic analysis identified nine clusters of nycteribiid bat flies on Madagascar and the neighbouring Comoros Archipelago. Bat flies sampled from frugivorous bats of the family Pteropodidae are monoxenous: Eucampsipoda madagascariensis, E. theodori and Cyclopodia dubia appear wholly restricted to Rousettus madagascariensis, R. obliviosus and Eidolon dupreanum, respectively. Two different host preference patterns occurred in nycteribiids infecting insectivorous bats. Flies parasitizing bats of the genera Miniopterus (Miniopteridae) and Myotis (Vespertilionidae), namely Penicillidia leptothrinax, Penicillidia sp. and Nycteribia stylidiopsis, are polyxenous and showed little host preference, while those parasitizing the genera Pipistrellus and Scotophilus (both Vespertilionidae) and referable to Basilia spp., are monoxenous. Lastly, the inferred Bayesian phylogeny revealed that the genus Basilia, as currently configured, is paraphyletic. CONCLUSION:This study provides new information on the differentiation of nycteribiid taxa, including undescribed species. Host preference is either strict as exemplified by flies parasitizing fruit bats, or more relaxed as found on some insectivorous bat species, possibly because of roost site sharing. Detailed taxonomic work is needed to address three undescribed nycteribiid taxa found on Pipistrellus and Scotophilus, tentatively allocated to the genus Basilia, but possibly warranting different generic allocation.
Project description:Most vertebrates host a wide variety of haematophagous parasites, which may play an important role in the transmission of vector-borne microorganisms to hosts. Surveillance is usually performed by collecting blood and/or tissue samples from vertebrate hosts. There are multiple methods to obtain samples, which can be stored for decades if properly kept. However, blood sampling is considered an invasive method and may possibly be harmful to the sampled individual. In this study, we investigated the use of ectoparasites as a tool to acquire molecular information about the presence and diversity of infectious microorganism in host populations. We tested the presence of three distinct vector-borne microorganisms in both bat blood and bat flies: Bartonella bacteria, malaria-like Polychromophilus sp. (Apicomplexa), and Trypanosoma sp. (Kinetoplastea). We detected the presence of these microorganisms both in bats and in their bat flies, with the exception of Trypanosoma sp. in South African bat flies. Additionally, we found Bartonella sp. in bat flies from one population in Spain, suggesting its presence in the host population even if not detected in bats. Bartonella and Polychromophilus infection showed the highest prevalence in both bat and bat fly populations. Single, co- and triple infections were also frequently present in both. We highlight the use of haematophagous ectoparasites to study the presence of infectious microorganism in host blood and its use as an alternative, less invasive sampling method.
Project description:BackgroundBats are hosts for many ectoparasites and act as reservoirs for several infectious agents, some of which exhibit zoonotic potential. Here, species of bats and bat flies were identified and screened for microorganisms that could be mediated by bat flies.MethodsBat species were identified on the basis of their morphological characteristics. Bat flies associated with bat species were initially morphologically identified and further identified at the genus level by analyzing the cytochrome c oxidase subunit I gene. Different vector-borne pathogens and endosymbionts were screened using PCR to assess all possible relationships among bats, parasitic bat flies, and their associated organisms.ResultsSeventy-four bat flies were collected from 198 bats; 66 of these belonged to Nycteribiidae and eight to Streblidae families. All Streblidae bat flies were hosted by Rhinolophus ferrumequinum, known as the most common Korean bat. Among the 74 tested bat flies, PCR and nucleotide sequencing data showed that 35 (47.3%) and 20 (27.0%) carried Wolbachia and Bartonella bacteria, respectively, whereas tests for Anaplasma, Borrelia, Hepatozoon, Babesia, Theileria, and Coxiella were negative. Phylogenetic analysis revealed that Wolbachia endosymbionts belonged to two different supergroups, A and F. One sequence of Bartonella was identical to that of Bartonella isolated from Taiwanese bats.ConclusionsThe vectorial role of bat flies should be checked by testing the same pathogen and bacterial organisms by collecting blood from host bats. This study is of great interest in the fields of disease ecology and public health owing to the bats' potential to transmit pathogens to humans and/or livestock.
Project description:Bat flies (Hippoboscoidea: Nycteribiidae and Streblidae) are obligate hematophagous ectoparasites of bats. We collected streblid bat flies from the New World (México) and the Old World (Uganda), and used metagenomics to identify their viruses. In México, we found méjal virus (Rhabdoviridae; Vesiculovirus), Amate virus (Reoviridae: Orbivirus), and two unclassified viruses of invertebrates. Méjal virus is related to emerging zoonotic encephalitis viruses and to the agriculturally important vesicular stomatitis viruses (VSV). Amate virus and its sister taxon from a bat are most closely related to mosquito- and tick-borne orbiviruses, suggesting a previously unrecognized orbivirus transmission cycle involving bats and bat flies. In Uganda, we found mamucuso virus (Peribunyaviridae: Orthobunyavirus) and two unclassified viruses (a rhabdovirus and an invertebrate virus). Mamucuso virus is related to encephalitic viruses of mammals and to viruses from nycteribiid bat flies and louse flies, suggesting a previously unrecognized orthobunyavirus transmission cycle involving hippoboscoid insects. Bat fly virus transmission may be neither strictly vector-borne nor strictly vertical, with opportunistic feeding by bat flies occasionally leading to zoonotic transmission. Many "bat-associated" viruses, which are ecologically and epidemiologically associated with bats but rarely or never found in bats themselves, may actually be viruses of bat flies or other bat ectoparasites.
Project description:The study of parasites in recently established populations of invasive species can shed light on the sources of invasion and possible indirect interactions between the alien species and native ones. We studied parasites of the global invader Harmonia axyridis (Coleoptera: Coccinellidae) in the Caucasus. In 2012, the first established population of Ha. axyridis was recorded in the Caucasus in Sochi (south of European Russia, Black Sea coast). By 2018, the ladybird had spread to a vast area: Armenia, Georgia and south Russia (Adygea, the Krasnodar territory, the Stavropol territory, Dagestan, Kabardino-Balkaria and North Ossetia). The examination of 213 adults collected in Sochi in 2018 showed that 53% were infested with Hesperomyces virescens fungi (Ascomycota: Laboulbeniales) and that 8% were infested with Parasitylenchus bifurcatus nematodes (Nematoda: Tylenchida, Allantonematidae). The examined Ha. axyridis specimens were free of the parasitic mite Coccipolipus hippodamiae. An analysis of the phylogenetic relationships of P. bifurcatus based on 18S rDNA confirmed the morphological identification of this species. Hesperomyces virescens and P. bifurcatus were first recorded in the Caucasus and Russia, although they are rather widespread in Europe. This likely indicates that they appeared as a result of coinvasion with their host because the populations of Ha. axyridis, He. virescens and P. bifurcatus in the Caucasus are isolated from the main parts of the ranges of these species in Europe. The nearest localities of Ha. axyridis is on another shore of the Black Sea, and the nearest localities of He. virescens and P. bifurcatus are more than 1000 km from the Caucasus. It is impossible to determine whether the first founders of the Caucasian population were infested with the parasites or whether the parasites were introduced by specimens of Ha. axyridis that arrived later from Europe. Harmonia axyridis was released in the region for pest control, but laboratory cultures are always free of He. virescens and P. bifurcatus. Therefore, the detection of He. virescens and P. bifurcatus indicates that the population of Ha. axyridis in the Caucasus could not have derived exclusively from released specimens. We did not find He. virescens on 400 specimens of 29 other ladybird species collected from the same localities as Ha. axyridis in the Caucasus. No reliable correlation between infestation by He. virescens and that by P. bifurcatus has been found. In addition to these two parasites, an unidentified species of the order Mermithida was recorded. This is the first documented case of Ha. axyridis infestation by a parasitic nematode of this order in nature.
