On the Fly: Tritrophic Associations of Bats, Bat Flies, and Fungi

Abstract

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.

Focus on Hyperparasites: Biotic and Abiotic Traits Affecting the Prevalence of Parasitic Microfungi on Bat Ectoparasites

“…Most of the bat fly species collected in our study (8 out of 10) showed signs of Laboulbeniales infections (Table 1), although the parasite prevalence on three bat fly species is very low (<1%) and thus the infection may be considered rare. All infected bat fly species were already known to host Laboulbeniales fungi (Haelewaters et al, 2017;de Groot et al, 2020). The bat flies in our study were collected from a wide range of bat species in Bulgaria (nine bat species) and Romania (27 bat species).…”

“…In the study by Haelewaters et al (2017), parasite prevalence of N. schmidlii by A. eucampsipodae was 2.72% (4 of 147 bat flies infected). Arthrorhynchus eucampsipodae is much rarer than A. nycteribiae but has thus far been reported from twelve bat fly species in five genera (de Groot et al, 2020). However, these data are misleading because recent work has shown that this taxon consists of multiple species that are host specific (Haelewaters et al, 2020).…”

“…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, , 2018(Haelewaters et al, , 2021bde Groot et al, 2020).…”

“…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).…”

DarkCideS 1.0, a global database for bats in karsts and caves

“…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 .…”