Parasites of parasites of bats: Laboulbeniales (Fungi: Ascomycota) on bat flies (Diptera: Nycteribiidae) in central Europe

Abstract

BackgroundBat 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).ResultsWe 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.ConclusionsWe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2022-y) contains supplementary material, which is available to authorized users.

Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations

“…Our complete dataset, prior to excluding specimens and partitioning (), was composed of 2,599 bats and 7,949 bat flies, of which 363 (= 4.6%) were infected by Laboulbeniales. Seven bat species were included in our final temperate dataset (Haelewaters et al., 2017a; Szentiványi et al., ). The most abundantly parasitized bat species was Miniopterus schreibersii ( n = 414), followed by Myotis daubentonii ( n = 206).…”

“…Included in this study were bat flies from Latin America [Costa Rica (T. Hiller, unpublished data), Ecuador, Mexico, Nicaragua (C.W. Dick, unpublished data), Honduras (Dick, ), Panama (Walker et al., ) and Trinidad (J.J. Camacho, unpublished data)] and Europe [Croatia, Hungary, Portugal, Slovakia, and Spain in Europe (Haelewaters et al., ; Szentiványi et al., )].…”

“…Our complete dataset, prior to excluding specimens and partitioning (Supporting Information), was composed of 2,599 bats and 7,949 bat flies, of which 363 (= 4.6%) were infected by Laboulbeniales. Seven bat species were included in our final temperate dataset (Haelewaters et al, 2017a;Szentiványi et al, 2018). In our neotropical dataset ( Figure 6) Notes.…”

“…Some of his publications presented species descriptions and new records for Arthrorhynchus , a genus apparently restricted to Old World bat flies (Thaxter, , , , , ), and two genera that thus far have only been reported on neotropical bat flies, Gloeandromyces and Nycteromyces (Thaxter, , , ). Until we initiated our studies on bat fly‐associated Laboulbeniales, five species were known from the type collections only (Haelewaters et al., 2017a, ; Walker et al., ). This illustrates how underexplored these hyperparasites are.…”

Morphological Species of Gloeandromyces (Ascomycota, Laboulbeniales) Evaluated Using Single-locus Species Delimitation Methods

“…The genus Dimeromyces, on the other hand, is one of the largest genera of Laboulbeniales encompassing 115 species, of which only two are found on bat flies (Rossi et al 2015. In the last few years, studies on bat fly-associated Laboulbeniales have focused on extensive surveying, taxonomy (description of species), host specificity, tripartite association networks, phylogenetic placement of bat fly-specific genera, and morphological versus molecular diversity of Gloeandromyces (Haelewaters et al 2017a, b, 2018b, Szentiványi et al 2018, Walker et al 2018.…”