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

Andrei Daniel Mihalca,Danny Haelewaters,Attila D. Sándor,Áron Péter

doi:10.3389/fevo.2022.795020

Abstract

The tritrophic association of bats, bat flies, and Laboulbeniales microfungi is a remarkably understudied system that may reveal patterns applicable to community ecology theory of (hyper)parasites. Laboulbeniales are biotrophic microfungi, exclusively associated with arthropods, with several species that are specialized on bat flies, which themselves are permanent ectoparasites of bats. Several hypotheses were tested on biotic and abiotic traits that may influence the presence and prevalence of hyperparasitic Laboulbeniales fungi on bat flies, based on southeastern European data. We found a wide distribution of fungal infection on bat flies, with underground-dwelling bats hosting more Laboulbeniales-infected flies compared to crevice-dwelling species. Bat host behavior, sociality, roost selection (underground versus crevice), bat fly sex, and season all have significant effects on the prevalence of fungal infection. Laboulbeniales infections are more common on bat flies that are infecting bat species with dense and long-lasting colonies (Miniopterus schreibersii, Myotis myotis, Myotis blythii), which roost primarily in underground sites. Inside these sites, elevated temperature and humidity may enhance the development and transmission of Laboulbeniales fungi. Sexual differences in bat hosts’ behavior also have an effect on fungal infection risk, with densely roosting female bat hosts harboring more Laboulbeniales-infected bat flies.

Highlights

Often neglected in biodiversity and conservation studies, parasites are among the most diverse modes of life
We found seasonal differences in the prevalence of Laboulbeniales infections on bat flies
We suggest to continuously measure temperature, humidity, and precipitation while surveying roosts for bats and their associated parasites and hyperparasites—to gain a better understanding of microhabitat conditions governing Laboulbeniales infections of flies collected from cave-dwelling bats

Summary

Introduction

Often neglected in biodiversity and conservation studies, parasites are among the most diverse modes of life. They are critical components of ecosystems, altering food webs, regulating population dynamics, and driving the evolution of other species (Windsor, 1995; Bush et al, 2001; Dougherty et al, 2016; Carlson et al, 2020). A special case of parasitism— and even more understudied—is hyperparasitism, the phenomenon of parasites exploiting other parasite species (Sullivan and Völkl, 1999). Hyperparasitism has an important role in regulating host–parasite cycles of natural populations, by shaping disease dynamics and other ecological. 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, 2018, 2021b; de Groot et al, 2020)

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Conclusion