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Bat flies (Nycteribiidae) of the order Diptera are highly specialized bloodsucking ectoparasites living on bats. The life-cycle of the bat flies emphasizes their obligate relationship with their hosts as they spend almost their entire life on bats. Upon mating, the female bat fly carries the larvae internally until the 3 rd -instar when it deposits the larvae on the ceiling of the roost occupied by bats. The larvae then form a puparium. After 3-4 weeks the adult bat fly emerges from the puparium and starts searching for a host bat to colonize.Some of these ectoparasitic bat flies themselves are infected with an ectoparasitic fungus of the genus  Arthrorhynchus  (Laboulbeniales). Ascospores of the fungi attach themselves to the cuticle of the bat fly and develop a very conspicuous haustorium that penetrates into the soft tissues from where it presumably extract nutrition from the hemolymph of the bat flies. This interaction converts the fungus into a hyperparasite. Both the parasite and hyperparasite are obligates and cannot live separate from their hosts. This peculiar case of hyperparasitism remains highly unknown.The bat flies were collected in caves of Portugal, in maternity and hibernation bat seasons, and in the autumn migration period. The most common species of cave-dwelling bat species in Portugal is  Miniopterus schreibersii , frequently parasitized with  Nycteribia schmidlii  and  Penicillidia conspicua  bat flies. We have studied the prevalence of the Laboulbeniales of the genus  Arthrorhynchus  in natural populations of bat flies. The site and position of the fungus on male and female bat flies unveils the mechanism of fungal transmission among bat flies, indicating that it occurs during mating behavior. This study is the starting point towards the understanding of this unique case of fungus-insect-vertebrate hyperparasitism interaction. See Suppl. material  1 .

Hyperparasitism in caves: bats, bat flies and ectoparasitic fungus