title: Parasites of parasites of bats: Laboulbeniales (Fungi: Ascomycota) on bat flies (Diptera: Nycteribiidae) in central Europe.
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.
authors.affiliation: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA. dhaelewaters@fas.harvard.edu.
authors.forename: Danny
authors.initials: D
authors.lastname: Haelewaters
authors.affiliation: Department of Biotechnology and Microbiology, University of Debrecen, Debrecen, Hungary.
authors.forename: Walter P
authors.initials: WP
authors.lastname: Pfliegler
authors.affiliation: Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary.|Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.|Museum of Zoology, Lausanne, Switzerland.
authors.forename: Tamara
authors.initials: T
authors.lastname: Szentiványi
authors.affiliation: Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary.
authors.forename: Mihály
authors.initials: M
authors.lastname: Földvári
authors.affiliation: Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania.
authors.forename: Attila D
authors.initials: AD
authors.lastname: Sándor
authors.affiliation: Romanian Bat Protection Association, Satu Mare, Romania.
authors.forename: Levente
authors.initials: L
authors.lastname: Barti
authors.affiliation: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA.
authors.forename: Jasmin J
authors.initials: JJ
authors.lastname: Camacho
authors.affiliation: Biometris, Wageningen University, Wageningen, The Netherlands.
authors.forename: Gerrit
authors.initials: G
authors.lastname: Gort
authors.affiliation: Department of Zoology, Eszterházy Károly University, Eger, Hungary.
authors.forename: Péter
authors.initials: P
authors.lastname: Estók
authors.affiliation: Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany.
authors.forename: Thomas
authors.initials: T
authors.lastname: Hiller
authors.affiliation: Department of Biology, Western Kentucky University, Bowling Green, Kentucky, USA.
authors.forename: Carl W
authors.initials: CW
authors.lastname: Dick
authors.affiliation: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA.
authors.forename: Donald H
authors.initials: DH
authors.lastname: Pfister
mesh_terms: D000818:Animals; D001203:Ascomycota / Q000145:classification / Q000235:genetics / Q000302:isolation & purification*; D002685:Chiroptera / Q000469:parasitology*; D004271:DNA, Fungal / Q000737:chemistry / Q000235:genetics; D004275:DNA, Ribosomal / Q000737:chemistry / Q000235:genetics; D004175:Diptera / Q000382:microbiology*; D006814:Hungary; D012383:Romania; D017422:Sequence Analysis, DNA
chemical_list: D004271:DNA, Fungal; D004275:DNA, Ribosomal
keywords: Arthrorhynchus; Bat flies; Ecological specificity; Ectoparasitic fungi; Host specificity; Hyperparasitism