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Bats, Bat Flies, and Fungi: Exploring Uncharted Waters

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Abstract

Bats serve as hosts to many lineages of arthropods, of which the blood-sucking bat flies (Nycteribiidae and Streblidae) are the most conspicuous. Bat flies can in turn be parasitized by Laboulbeniales fungi, which are biotrophs of arthropods. This is a second level of parasitism, hyperparasitism, a severely understudied phenomenon. Four genera of Laboulbeniales are known to occur on bat flies, Arthrorhynchus on Nycteribiidae in the Eastern Hemisphere, Dimeromyces on Old World Streblidae, Gloeandromyces on New World Streblidae, and Nycteromyces on Streblidae in both hemispheres. In this chapter, we introduce the different partners of the tripartite interaction and discuss their species diversity, ecology, and patterns of specificity. We cover parasite prevalence of Laboulbeniales fungi on bat flies, climatic effects on parasitism of bat flies, and coevolutionary patterns. One of the most important questions in this tripartite system is whether habitat has an influence on parasitism of bat flies by Laboulbeniales fungi. We hypothesize that habitat disturbance causes parasite prevalence to increase, in line with the “dilution effect.” This can only be resolved based on large, non-biased datasets. To obtain these, we stress the importance of multitrophic field expeditions and international collaborations.

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... Hyperparasitism has been well documented for many groups of organisms, mainly insect parasitoids associated with parasitoid hosts, viruses that parasitize disease-causing protozoans, and parasitic flowering plants (Grybchuk et al ., 2018;Krasylenko et al ., 2021;Sullivan, 1987). Hyperparasitism by fungi is poorly studied, even though it is thought to be rather widespread in nature (Haelewaters et al ., 2018a(Haelewaters et al ., , 2021aParratt and Laine, 2016;Sun et al ., 2019). As fungi are able to parasitize organisms from different kingdoms (Moore et al ., 2020), this chapter focuses on fungal hyperparasites parasitic on both fungal and non-fungal hosts. ...
... Twenty years later, Merola (1952) described a sixth species, and it took another 65 years for any taxonomic contributions in this system (Haelewaters et al ., 2017b). To date, 18 species in four genera are known to parasitize bat flies (Haelewaters et al ., 2021a;Liu et al ., 2020;Van Caenegem et al ., 2023;W. Van Caenegem and D. Haelewaters, unpublished data): four species of Arthrorhynchus , two species of Dimeromyces, ten species of Gloeandromyces, and two species of Nycteromyces (Fig. 8). ...
... Except some regional studies focusing on prevalence of parasites and one study reviewing tritrophic associations globally and analyzing host specificity patterns (de Groot et al ., 2020), other aspects remain unstudied. Efforts are being made towards a global tritrophic traits database to study some of these aspects based on records resulting from standardized fieldwork (Haelewaters et al ., 2021a). One question of interest is how environmental pressures such as changing landscapes and warming climate affect parasitism at these multiple levels. ...
Preprint
Even parasites have parasites. By definition, a hyperparasite is an organism capable of parasitizing another parasite. Hyperparasitism caused by fungi is a common phenomenon in nature, but it has been poorly studied. This life history strategy evolved several times in the fungal tree of life, and is crucial in the maintenance of ecosystems as well as in the mediation of parasite–host interactions. Although the interest for hyperparasitic fungi is growing in the context of biological control, hyperparasitism is not ecologically and evolutionarily understood. This chapter summarizes the most relevant aspects of the terminology, diversity, and ecology of hyperparasitic fungi on both fungal and non-fungal hosts. We also discuss the problems related to molecular research on hyperparasitic fungi. As they represent a hidden source of diversity, it is necessary to increase sampling efforts and to undertake further morphological, molecular, and ecological studies to understand these fungi and their potential biotechnological and pharmaceutical uses.
... Instead, through subsequent mitotic divisions, a two-celled ascospore develops into a microscopic, resilient structure of determinate growth: a thallus (Blackwell et al. 2020). The entire life cycle is completed on a single host (Haelewaters et al. 2021b). In addition, many Laboulbeniales are known to be host-specific. ...
... Representatives of four genera of Laboulbeniales are known to have bat fly hosts: Arthrorhynchus Kolen., Dimeromyces Thaxt., Gloeandromyces Thaxt., and Nycteromyces Thaxt. (de Groot et al. 2020;Haelewaters et al. 2021b). The prevalence of Laboulbeniales on bat flies is generally very low, ranging from 2.2% for nycteribiid bat flies in the Eastern Hemisphere up to 7% for streblid bat flies in the Western Hemisphere (Haelewaters et al. 2021b). ...
... (de Groot et al. 2020;Haelewaters et al. 2021b). The prevalence of Laboulbeniales on bat flies is generally very low, ranging from 2.2% for nycteribiid bat flies in the Eastern Hemisphere up to 7% for streblid bat flies in the Western Hemisphere (Haelewaters et al. 2021b). Throughout the 20th century, little research was done on bat fly-associated Laboulbeniales, since the multitrophic lifestyle and inconspicuous nature of these fungi make for a difficult study system. ...
Article
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This paper describes and illustrates five new species of Gloeandromyces (Ascomycota, Laboulbeniales) associated with tropical American bat flies (Diptera, Streblidae). These are Gloeandromyces cusucoensis sp. nov. from Trichobius uniformis in Costa Rica and Honduras, G. diversiformis sp. nov. from Strebla wiedemanni in Costa Rica, G. plesiosaurus sp. nov. from Trichobius yunkeri in Panama, G. pseudodickii sp. nov. from Trichobius longipes in Ecuador and Panama, and G. verbekeniae sp. nov. from Strebla galindoi in Ecuador and Panama. The description of these five species doubles the number of known species in the genus. Morphological characteristics, host association, and a three-locus (18S nuc rDNA, 28S nuc rDNA, TEF1) phylogenetic reconstruction support placement of these taxa in the genus Gloeandromyces. Three of the new species are polymorphic; they have multiple morphotypes that grow in specific positions on the host integument: G. diversiformis f. diversiformis, f. musiformis, and f. vanillicarpiformis; G. plesiosaurus f. asymmetricus and f. plesiosaurus; and G. verbekeniae f. verbekeniae and f. inflexus. Finally, a dichotomous key to all species and morphotypes is presented.
... -Laboulbeniales are obligate biotrophic fungi of arthropods. About 80 % of described Laboulbeniales taxa are known from beetles (Coleoptera), but these fungi are found on a wide variety of hosts, including ants (Hymenoptera: Formicidae), harvestmen (Opiliones), millipedes (Diplopoda), mites (Acari), true bugs (Hemiptera), and flies (Diptera)-including the ectoparasitic bat flies (Enghoff & Santamaría 2015;Haelewaters et al. 2017Haelewaters et al. , 2020aSantamaría et al. 2017). Bat flies are obligate hematophagous parasites of bats (Mammalia: Chiroptera) belonging to two families, Nycteribiidae and Streblidae. ...
... and Nycteromyces Thaxt. (Dogonniuck et al. 2019, Haelewaters et al. 2020a. Arthrorhynchus species are restricted to the Eastern Hemisphere. ...
... Bat flies are a suitable model to study host-parasite associations under the 'Stockholm paradigm' framework. They are divided into two cosmopolitan dipteran families of obligate ectoparasites of bats, Streblidae and Nycteribiidae (Diptera: Hippoboscoidea), although their taxonomic status is under debate (Dittmar et al., 2015;Haelewaters et al., 2021). Bat flies are often presented as highly specialized, particularly those on Neotropical bats (Haelewaters et al., 2021). ...
... They are divided into two cosmopolitan dipteran families of obligate ectoparasites of bats, Streblidae and Nycteribiidae (Diptera: Hippoboscoidea), although their taxonomic status is under debate (Dittmar et al., 2015;Haelewaters et al., 2021). Bat flies are often presented as highly specialized, particularly those on Neotropical bats (Haelewaters et al., 2021). There are even hypotheses regarding the possibility of cospeciation between bats and bat flies in the Western Hemisphere (Patterson et al., 1998). ...
Article
The genus Noctiliostrebla Wenzel (Diptera: Streblidae) stands out for its high degree of specificity exhibited in relation to bat species of the genus Noctilio Linnaeus and provides an exciting system for understanding the history behind host–parasite associations. Here, we present a phylogeny of Noctiliostrebla based on an analysis of DNA sequences and morphological characters, along with cophylogenetic and biogeographical analyses. Our results strongly support the monophyly of Noctiliostrebla, but with uncertainties within the genus. With a low frequency of cospeciation events explaining the associations between hosts and parasites, cophylogenetic analyses did not show an overall congruence between the host and parasite phylogenies. Indeed, two parallel histories were recovered in the host–parasite associations, which might indicate that niche segregation is determined evolutionarily, facilitating the coexistence of parasites and promoting diversification. Biogeographical analysis showed a strong spatial congruence between disjunct distributions of Noctiliostrebla and major river basins in South America and with areas of higher elevation, which might be associated with the glacial periods throughout the Pliocene and Pleistocene. Overall, our findings suggest an agreement with the expectations of the ‘Stockholm paradigm’ framework, in which biogeographical events and ecological factors act as important components to explain the associations, instead of cospeciation events.
... -Laboulbeniales are obligate biotrophic fungi of arthropods. About 80 % of described Laboulbeniales taxa are known from beetles (Coleoptera), but these fungi are found on a wide variety of hosts, including ants (Hymenoptera: Formicidae), harvestmen (Opiliones), millipedes (Diplopoda), mites (Acari), true bugs (Hemiptera), and flies (Diptera)-including the ectoparasitic bat flies (Enghoff & Santamaría 2015;Haelewaters et al. , 2020aSantamaría et al. 2017). Bat flies are obligate hematophagous parasites of bats (Mammalia: Chiroptera) belonging to two families, Nycteribiidae and Streblidae. ...
... and Nycteromyces Thaxt. (Dogonniuck et al. 2019, Haelewaters et al. 2020a. Arthrorhynchus species are restricted to the Eastern Hemisphere. ...
Article
Fungal Systematics and Evolution (FUSE) is one of the journal series to address the “fusion” between morphological data and molecular phylogenetic data and to describe new fungal taxa and interesting observations. This paper is the 6th contribution in the FUSE series—presenting one new genus, twelve new species, twelve new country records, and three new combinations. The new genus is: Pseudozeugandromyces (Laboulbeniomycetes, Laboulbeniales). The new species are: Albatrellopsis flettioides from Pakistan, Aureoboletus garciae from Mexico, Entoloma canadense from Canada, E. frigidum from Sweden, E. porphyroleucum from Vietnam, Erythrophylloporus flammans from Vietnam, Marasmiellus boreoorientalis from Kamchatka Peninsula in the Russian Far East, Marasmiellus longistipes from Pakistan, Pseudozeugandromyces tachypori on Tachyporus pusillus (Coleoptera, Staphylinidae) from Belgium, Robillarda sohagensis from Egypt, Trechispora hondurensis from Honduras, and Tricholoma kenanii from Turkey. The new records are: Arthrorhynchus eucampsipodae on Eucampsipoda africanum (Diptera, Nycteribiidae) from Rwanda and South Africa, and on Nycteribia vexata (Diptera, Nycteribiidae) from Bulgaria; A. nycteribiae on Eucampsipoda africanum from South Africa, on Penicillidia conspicua (Diptera, Nycteribiidae) from Bulgaria (the first undoubtful country record), and on Penicillidia pachymela from Tanzania; Calvatia lilacina from Pakistan; Entoloma shangdongense from Pakistan; Erysiphe quercicola on Ziziphus jujuba (Rosales, Rhamnaceae) and E. urticae on Urtica dioica (Rosales, Urticaceae) from Pakistan; Fanniomyces ceratophorus on Fannia canicularis (Diptera, Faniidae) from the Netherlands; Marasmiellus biformis and M. subnudus from Pakistan; Morchella anatolica from Turkey; Ophiocordyceps ditmarii on Vespula vulgaris (Hymenoptera, Vespidae) from Austria; and Parvacoccum pini on Pinus cembra (Pinales, Pinaceae) from Austria. The new combinations are: Appendiculina gregaria, A. scaptomyzae, and Marasmiellus rodhallii. Analysis of an LSU dataset of Arthrorhynchus including isolates of A. eucampsipodae from Eucampsipoda africanum and Nycteribia spp. hosts, revealed that this taxon is a complex of multiple species segregated by host genus. Analysis of an SSU–LSU dataset of Laboulbeniomycetes sequences revealed support for the recognition of four monophyletic genera within Stigmatomyces sensu lato: Appendiculina, Fanniomyces, Gloeandromyces, and Stigmatomyces sensu stricto. Finally, phylogenetic analyses of Rhytismataceae based on ITS–LSU ribosomal DNA resulted in a close relationship of Parvacoccum pini with Coccomyces strobi.
... -Laboulbeniales are obligate biotrophic fungi of arthropods. About 80 % of described Laboulbeniales taxa are known from beetles (Coleoptera), but these fungi are found on a wide variety of hosts, including ants (Hymenoptera: Formicidae), harvestmen (Opiliones), millipedes (Diplopoda), mites (Acari), true bugs (Hemiptera), and flies (Diptera)-including the ectoparasitic bat flies (Enghoff & Santamaría 2015;Haelewaters et al. 2017Haelewaters et al. , 2020aSantamaría et al. 2017). Bat flies are obligate hematophagous parasites of bats (Mammalia: Chiroptera) belonging to two families, Nycteribiidae and Streblidae. ...
... and Nycteromyces Thaxt. (Dogonniuck et al. 2019, Haelewaters et al. 2020a. Arthrorhynchus species are restricted to the Eastern Hemisphere. ...
... -Laboulbeniales are obligate biotrophic fungi of arthropods. About 80 % of described Laboulbeniales taxa are known from beetles (Coleoptera), but these fungi are found on a wide variety of hosts, including ants (Hymenoptera: Formicidae), harvestmen (Opiliones), millipedes (Diplopoda), mites (Acari), true bugs (Hemiptera), and flies (Diptera)-including the ectoparasitic bat flies (Enghoff & Santamaría 2015;Haelewaters et al. , 2020aSantamaría et al. 2017). Bat flies are obligate hematophagous parasites of bats (Mammalia: Chiroptera) belonging to two families, Nycteribiidae and Streblidae. ...
... and Nycteromyces Thaxt. (Dogonniuck et al. 2019, Haelewaters et al. 2020a. Arthrorhynchus species are restricted to the Eastern Hemisphere. ...
Article
Full-text available
Fungal Systematics and Evolution (FUSE) is one of the journal series to address the “fusion” between morphological data and molecular phylogenetic data and to describe new fungal taxa and interesting observations. This paper is the 6th contribution in the FUSE series—presenting one new genus, twelve new species, twelve new country records, and three new combinations. The new genus is: Pseudozeugandromyces (Laboulbeniomycetes, Laboulbeniales). The new species are: Albatrellopsis flettioides from Pakistan, Aureoboletus garciae from Mexico, Entoloma canadense from Canada, E. frigidum from Sweden, E. porphyroleucum from Vietnam, Erythrophylloporus flammans from Vietnam, Marasmiellus boreoorientalis from Kamchatka Peninsula in the Russian Far East, Marasmiellus longistipes from Pakistan, Pseudozeugandromyces tachypori on Tachyporus pusillus (Coleoptera, Staphylinidae) from Belgium, Robillarda sohagensis from Egypt, Trechispora hondurensis from Honduras, and Tricholoma kenanii from Turkey. The new records are: Arthrorhynchus eucampsipodae on Eucampsipoda africanum (Diptera, Nycteribiidae) from Rwanda and South Africa, and on Nycteribia vexata (Diptera, Nycteribiidae) from Bulgaria; A. nycteribiae on Eucampsipoda africanum from South Africa, on Penicillidia conspicua (Diptera, Nycteribiidae) from Bulgaria (the first undoubtful country record), and on Penicillidia pachymela from Tanzania; Calvatia lilacina from Pakistan; Entoloma shangdongense from Pakistan; Erysiphe quercicola on Ziziphus jujuba (Rosales, Rhamnaceae) and E. urticae on Urtica dioica (Rosales, Urticaceae) from Pakistan; Fanniomyces ceratophorus on Fannia canicularis (Diptera, Faniidae) from the Netherlands; Marasmiellus biformis and M. subnudus from Pakistan; Morchella anatolica from Turkey; Ophiocordyceps ditmarii on Vespula vulgaris (Hymenoptera, Vespidae) from Austria; and Parvacoccum pini on Pinus cembra (Pinales, Pinaceae) from Austria. The new combinations are: Appendiculina gregaria, A. scaptomyzae, and Marasmiellus rodhallii. Analysis of an LSU dataset of Arthrorhynchus including isolates of A. eucampsipodae from Eucampsipoda africanum and Nycteribia spp. hosts, revealed that this taxon is a complex of multiple species segregated by host genus. Analysis of an SSU–LSU dataset of Laboulbeniomycetes sequences revealed support for the recognition of four monophyletic genera within Stigmatomyces sensu lato: Appendiculina, Fanniomyces, Gloeandromyces, and Stigmatomyces sensu stricto. Finally, phylogenetic analyses of Rhytismataceae based on ITS–LSU ribosomal DNA resulted in a close relationship of Parvacoccum pini with Coccomyces strobi.
... -Laboulbeniales are obligate biotrophic fungi of arthropods. About 80 % of described Laboulbeniales taxa are known from beetles (Coleoptera), but these fungi are found on a wide variety of hosts, including ants (Hymenoptera: Formicidae), harvestmen (Opiliones), millipedes (Diplopoda), mites (Acari), true bugs (Hemiptera), and flies (Diptera)-including the ectoparasitic bat flies (Enghoff & Santamaría 2015;Haelewaters et al. , 2020aSantamaría et al. 2017). Bat flies are obligate hematophagous parasites of bats (Mammalia: Chiroptera) belonging to two families, Nycteribiidae and Streblidae. ...
... and Nycteromyces Thaxt. (Dogonniuck et al. 2019, Haelewaters et al. 2020a. Arthrorhynchus species are restricted to the Eastern Hemisphere. ...
... Emerging technologies and trends in scientific data collection may make significant contributions towards addressing knowledge gaps in poorly studied groups (Hortal et al., 2015). For example, standardized multitrophic, multiyear, and multisite monitoring programs have been proposed to build large-scale datasets to address current knowledge gaps (species distributions, abiotic tolerances, etc.) of poorly studied groups (Haelewaters, Dick, et al., 2021). In addition, citizen science may prove a powerful tool for sourcing biological data on poorly studied taxa on a scale that formal scientific surveys are not capable of (Irga et al., 2018). ...
Article
Most empirical research on biological shortfalls has focused on vertebrate taxa. This is important given many species in poorly studied groups such as invertebrates, plants, and fungi are predicted to possess high conservation risk. Here, we focus on Laboulbeniomycetes: a class of microfungi that are understudied. We examined four shortfalls: Linnean (knowledge gaps in species diversity), Wallacean (knowledge gaps in distributions), Latimerian (knowledge gaps in species persistence), and the newly introduced Scottian (knowledge gaps in species conservation assessments) shortfalls. The Linnean shortfall in Laboulbeniomycetes is hard to predict due to inconsistent species description rates. Analysis of distribution patterns indicates Laboulbeniomycetes are likely to experience an extremely high Wallacean shortfall, with many species having highly disjunct known distributions. Latimerian shortfall analysis shows over half (51%) of Laboulbeniomycetes have not been recorded in >50 years, while the group has a collective Scottian shortfall of 100%, given none of the 2454 described species have received an IUCN threat assessment. We suggest continued study of natural history collections, expanded citizen science programmes, and machine-learning identification approaches as important tools for reducing knowledge shortfalls in both Laboulbeniomycetes and poorly studied taxa more generally.
... Thus, fungal pathogens can be transferred between land-use types with relative ease. Finally, bats host highly specialized parasites with the potential to not only spread pathogens within a bat colony, but also host their own unique fungi, including ectoparasitic ones [28][29][30], with some studies finding 43% of bat flies hosting fungi. Bat parasites include mites, ticks, fleas, and bat flies (streblids, nycteribiids, and ascodipterans). ...
Article
Fungal pathogens have become an increasingly important topic in recent decades. Yet whilst various cankers and blights have gained attention in temperate woodlands and crops, the scope for fungal pathogens of animals and their potential threat has received far less attention. With a shifting climate, the threat from fungal pathogens is predicted to increase in the future, thus understanding the spread of fungi over landscapes as well as taxa that may be at risk is of particular importance. Cave ecosystems provide potential refugia for various fungi, and roosts for bats. With their well vascularized wings and wide-ranging distributions, bats present potential fungal vectors. Furthermore, whilst bat immune systems are generally robust to bacterial and viral pathogens, they can be susceptible to fungal pathogens, particularly during periods of stress such as hibernation. Here we explore why bats are important and interesting vectors for fungi across landscapes and discuss knowledge gaps that require further research.
... The term hyperparasite refers to an organism that parasitizes another parasitic organism. Hyperparasitism caused by fungi is rather widespread in nature, but it is a phenomenon that has been poorly studied (Haelewaters et al., 2018a(Haelewaters et al., , 2021. Several authors have reviewed this type of interaction (Barnett, 1963;Boosalis, 1964;Barnett and Binder, 1973;Cooke, 1977;Hawksworth, 1981;Haelewaters et al., 2018b;Sun et al., 2019). ...
Article
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Hyperparasitism on plant-parasitic fungi is a widespread but rarely studied phenomenon. Here, for the first time, we compile in a checklist information provided by peer-reviewed literature for fungi growing on colonies of black mildews (Meliolales, Ascomycota), a species-rich group of tropical and subtropical plant-parasitic microfungi. The checklist contains information on 189 species of contact-biotrophic microfungi in 82 genera. They belong to seven morphological groups: dematiaceous hyphomycetes, moniliaceous hyphomycetes, pycnidioid, perithecioid, catathecioid, and apothecioid fungi. By the fact that species accumulation curves do not reach saturation for any tropical country, it is evident that the knowledge of the diversity of hyperparasitic fungi on Meliolales is incomplete. A network analysis of records of hyperparasitic fungi, their host fungi and host plants shows that genera of hyperparasitic fungi are generalists concerning genera of Meliolales. However, most species of hyperparasitic fungi are restricted to meliolalean hosts. In addition to hyperparasitic fungi, diverse further microorganisms use meliolalean colonies as ecological niche. Systematic positions of most species are unknown because DNA sequence data are lacking for species of fungi hyperparasitic on Meliolales. We discuss the specific challenges of obtaining DNA sequence data from hyperparasitic fungi. In order to better understand the diversity, evolution and biology of hyperparasitic fungi, it is necessary to increase sampling efforts and to undertake further morphological, molecular, and ecological studies.
... Bat fly taxonomy followed Dick and Graciolli 42 and Graciolli and Dick 43 and fungal taxonomy followed Index Fungorum 44 . In addition to the conspicuous bat flies, bats are host to several other lineages of parasites mites and ticks, lice, fleas, bugs, and earwigs 45,46 . Consequently, the fourth dataset will be expanded on in future versions of DarkCideS with data on these parasitic organisms. ...
Preprint
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Understanding biodiversity patterns as well as drivers of population declines, and range losses provides crucial baselines for monitoring and conservation. However, the information needed to evaluate such trends remains unstandardised and sparsely available for many taxonomic groups and habitats, including the cave-dwelling bats and cave ecosystems. Here, we present the DarkCideS 1.0 , a global database of bat caves and bat species based on curated data from the literature, personal collections, and existing datasets. The database contains information for geographical distribution, ecological status, species traits, and parasites and hyperparasites for 679 bat species known to occur in caves or use caves in their life-histories. The database contains 6746 georeferenced occurrences for 402 cave-dwelling bat species from 2002 cave sites in 46 countries and 12 terrestrial biomes. The database has been developed to be a collaborative, open-access, and user-friendly platform, allowing continuous data-sharing among the community of bat researchers and conservation biologists. The database has a range of potential applications in bat research and enables comparative monitoring and prioritisation for conservation.
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Global biodiversity and ecosystem function are the result of complex networks of interactions and feedbacks between animals and their environments, which in turn are affected by the interactions and feedbacks between animals and the organisms they host. Understanding these complex networks, including the main drivers of and responses to ecological and environmental changes and their global implications, requires adopting a systems-based perspective. We advocate for this approach by characterizing a framework centered around bats, a globally-distributed mammalian order, and their dual roles as both inhabitants of ecosystems and as habitats themselves. Like other organisms, bats interact with habitats by providing ecosystem services that impact the survival and distribution of other species, and may be affected by such factors as land use change, climate change, fluctuations in food availability, and hunting pressure. Habitat conditions (e.g. food availability, temperature, etc.) can affect the physiological condition of individuals, which in turn can affect the prevalence and/or virulence of hosted organisms and potential pathogens (e.g. ectoparasites, bacteria, viruses, fungi, and protozoa). In addition, the interactions among individuals (e.g. co-roosting, migration, etc.) influence the habitat connectivity for their hosted organisms (e.g. opportunities for dispersal). Bats have a unique relationship with infectious disease, both biological and cultural. With this in mind, when applied to bats this framework has special importance to how we understand and apply the One Health concept, whereby healthy natural environments foster both human and animal health, which in turn also promotes healthy environments. By leveraging a hierarchical approach among these different levels of biological organization, we can arrive at a clearer picture of the specific threats facing bats—as well as the risk of pathogen spillover to humans and other domesticated and wild animals generated by disrupting this delicate balance—and identify possible measures to mitigate adverse impacts. Thus, to understand these complex interactions and their implications for conservation, ecosystem health, and human health, we need a new ecological framework that recognizes that changes in habitats not only affect macrofauna and the ecosystem services they provide, but also have the potential to cascade through the diversity and evolution of the organisms they host. This review provides a case study for the application of this framework, which is extensible to other organisms with their own unique relationships with habitats and as habitats.
Chapter
Phylogenetic studies of Laboulbeniomycetes support recognition of three orders (Herpomycetales, Laboulbeniales, Pyxidiophorales) and two unnamed clades containing conidial, arthropod-associated fungi and a poorly known perithecial genus, Subbaromyces. Herpomycetales and Laboulbeniales include obligate arthropod-associated biotrophs characterized by a parenchymatous thallus of several thousand cells. Pyxidiophorales are hyphal mycoparasites with an unusual three-morph life cycle. The two-celled ascospore with a distinctive apparatus for attachment to arthropods ties together all Laboulbeniomycetes. The complex morphologies and life histories of these fungi are described as a background for research directions that will rely heavily on molecular methods, including phylogenomics, with emphasis on host–parasite relations.
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In this paper we present an updated checklist of thallus-forming Laboulbeniomycetes (Ascomycota, Pezi-zomycotina), that is, the orders Herpomycetales and Laboulbeniales, from Belgium and the Netherlands. Two species are newly described based on morphology, molecular data (ITS, LSU ribosomal DNA) and ecology (host association). These are Hesperomyces halyziae on Halyzia sedecimguttata (Coleoptera, Coc-cinellidae) from both countries and Laboulbenia quarantenae on Bembidion biguttatum (Coleoptera, Car-abidae) from Belgium. In addition, nine new country records are presented. For Belgium: Laboulbenia aubryi on Amara aranea (Coleoptera, Carabidae) and Rhachomyces spinosus on Syntomus foveatus (Co-leoptera, Carabidae). For the Netherlands: Chitonomyces melanurus on Laccophilus minutus (Coleoptera, Dytiscidae), Euphoriomyces agathidii on Agathidium laevigatum (Coleoptera, Leiodidae), Laboulbenia fas-ciculata on Omophron limbatum (Coleoptera, Carabidae), Laboulbenia metableti on Syntomus foveatus and S. truncatellus (Coleoptera, Carabidae), Laboulbenia pseudomasei on Pterostichus melanarius (Coleoptera, Carabidae), Rhachomyces canariensis on Trechus obtusus (Coleoptera, Carabidae), and Stigmatomyces hydrel-liae on Hydrellia albilabris (Diptera, Ephydridae). Finally, an identification key to 140 species of thallus-forming Laboulbeniomycetes in Belgium and the Netherlands is provided. Based on the combined data, we are able to identify mutual gaps that need to be filled as well as weigh the impact of chosen strategies (fieldwork, museum collections) and techniques in these neighboring countries. The aim of this work is to serve as a reference for studying Laboulbeniomycetes fungi in Europe.
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Background: Bat flies (Diptera: Nycteribiidae and Streblidae) are obligate, blood-sucking ectoparasites of bats with specialized morphology, life-cycle and ecology. Bat flies are occasionally infected by different species of Laboulbeniales (Fungi: Ascomycota), microscopic fungal ectoparasites belonging to three genera: Arthrorynchus spp. are restricted to the Eastern Hemisphere, while species of Gloeandromyces and Nycteromyces occur on Neotropical bat flies. Little is known about the distribution and host specificity of Arthrorynchus spp. on bat flies. In this study, we focused on sampling bat flies from the cave-dwelling bat species Miniopterus schreibersii. Bat and ectoparasite collection took place in Albania, Croatia, Hungary, Italy, Portugal, Slovakia, Spain and Switzerland. Flies were inspected for Laboulbeniales infections. Results: Six hundred sixty seven bat flies of five species were collected: Nycteribia latreillii, N. pedicularia, N. schmidlii, Penicillidia conspicua, and P. dufourii. Laboulbeniales infection was observed on 60 specimens (prevalence = 9%). Two Laboulbeniales species, Arthrorhynchus eucampsipodae and A. nycteribiae, were present on three bat fly species. All observations of A. eucampsipodae were on N. schmidlii, and A. nycteribiae was present on P. conspicua and P dufourii. Arthrorhynchus eucampsipodae is, for the first time, reported from Slovakia and Spain. Arthrorhynchus nycteribiae represents a new country record for Portugal and Slovakia. There were no significant differences among infection rates in different countries. Females of N. schmidlii showed a higher infection rate than males with an observable trend (P = 0.0502). No sex differences in infection rate for P. conspicua and P. dufourii were detected. Finally, thallus density was significantly lower in N. schmidlii compared to P. conspicua and P. dufourii. Conclusions: With this study, we contribute to the knowledge of the geographical distribution and host specificity of Laboulbeniales fungi associated with ectoparasitic bat flies within Europe. We discuss parasite prevalence and host specificity in the light of our findings and the available literature. Penicillidia conspicua is unambiguously the main host species for A. nycteribiae based on our and previous findings. Differences in parasite intensity and sex-biased infections of the fungi are possible depending on the species.
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The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere (Arthrorhynchus) and twice in the Western Hemisphere (Gloeandromyces, Nycteromyces). We hypothesize that the genera Arthrorhynchus and Nycteromyces evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus Gloeandromyces by considering the LSU rDNA region. Phenotypic plasticity and position-induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, G. pageanus and G. streblae, show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.
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Background: 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). Results: 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. Conclusions: 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.
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Two new species of yellow-shouldered bats Sturnira Gray, 1842 (Chiroptera, Phyllostomidae) from Central America and western South America are described using molecular and morphological data. The two new species, which occur in Costa Rica and Panama and in western Ecuador, were previously confused with S. ludovici, and S. lilium and S. luisi, respectively. Sturnira now includes 22 described species, making it the most speciose genus in the Neotropical family Phyllostomidae.
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A new species of Dimeromyces (Ascomycota, Laboulbeniales) parasitic on the bee louse Braula coeca Nitzsch (Diptera, Braulidae) is described. The most obvious differences between the new species and the others are the more inflated and more numerous antheridia (up to ten), the longer appendages, and the distinctly truncate perithecial apex. The fungus appears to be relatively common in the Czech Republic, with an infection rate of 12.6% (n = 372).
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Host specificity gauges the degree to which a parasite occurs in association with host species and is among the most fundamental properties of parasite–host associations. The degree of specificity is indicative of myriad properties of the host and parasite and of their ecological and evolutionary relationships. Bat flies are highly specialized bloodfeeding ectoparasites of bats worldwide and were historically viewed as unspecific. In the bat fly—bat system, numerous properties actually or potentially interrupt the linkage of parasite to host and should thus decrease specificity. Such properties of bat flies include a life history strategy requiring females to leave the host, an off-host pupal stage, and high dispersal capability of many species. For hosts, properties include high diversity, mobility, sociality, and multispecies roosting environments. These and other biological and ecological characteristics of bats and flies should together facilitate interspecific host transfers and over time lead to nonspecific host–parasite associations. Despite these properties, large and carefully executed biodiversity surveys of mammals and parasites unequivocally demonstrate the high host specificity of many bat flies, and molecular sequence data promise to demonstrate that many cases of lowered specificity are misunderstood due to unresolved parasite species boundaries. On the other hand, experimental approaches have suggested that host specificity is context dependent and may be lessened in cases of ecological disturbance and in particular when novel host–parasite associations are created. Evolution and maintenance of specificity in bat flies depends in part on the encounter and compatibility properties of bats and on the reproductive potential of the flies on available host species. Moreover, the degree to which parasites have coevolved immunological compatibility with their hosts, thereby diminishing immunological surveillance and response, may also serve to maintain high host specificity. Although worldwide bat species on average harbor higher diversity of parasites and pathogens than any other mammalian group, the likelihood of bat flies vectoring disease agents across host species of bats, and particularly to distantly related mammals such as humans, may be relatively small.
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In this paper, new species and formae of the genus Gloeandromyces (Ascomycota, Laboulbeniales) are described and illustrated. These are: Gloeandromyces dickii sp. nov. on Trichobius joblingi from Nicaragua and Panama; G. pageanus f. alarum f. nov. on Tri. joblingi from Panama; G. pageanus f. polymorphus f. nov. on Tri. dugesioides and Tri. joblingi from Panama and Trinidad; and G. streblae f. sigmomorphus f. nov. on Tri. joblingi from Panama. Gloeandromyces pageanus on Tri. dugesioides from Panama as described in Nova Hedwigia 105 (2017) is referred to as G. pageanus f. pageanus. Support for these descriptions of species and formae comes from phylogenetic reconstruction of the large subunit ribosomal DNA and from the application of species delimitation methods (ABGD, bPTP, GMYC). Host specialization results in phylogenetic segregation by host species in both G. pageanus and G. streblae and this may represent a case of incipient speciation. A second mechanism driving diversity involves position induced morphological adaptations, leading to the peculiar morphotypes that are associated to growing on a particular position of the integument (G. pageanus f. alarum, G. streblae f. sigmomorphus).
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Experiments were carried out with Laboulbenia slackensis (Ascomycetes, Laboulbeniales), an ectoparasitic univorous fungus of Pogonus chalceus (Coleoptera, Carabidae). Relative growth of Laboulbenia slackensis populations was significantly affected by environmental conditions, i.e., the soil composition, under which the typical host was reared. Optimal conditions for the development of the fungus corresponded with the optimal habitat selected by the typical host, i.e., pure salt marsh clay. Artificial infections with L. slackensis showed that the fungus was potentially plurivorous on Carabidae and that its specificity was not fully accounted for by the host physiology or integumental characteristics. L. slackensis was successfully transferred to 19 atypical carabid host species, and the morphological characteristics used to differentiate it from related taxa are stable on these hosts. As with the typical host, successful establishment of L. slackensis on an atypical host also depended on the soil composition under which the atypical host was reared. The host was essential, but alone not sufficient, for the establishment of the fungus. It is postulated that the specificity of L. slackensis observed in nature depends both on its host specificity and environmental preferences. Specialization of L. slackensis probably was the result of reinforced ecological isolation caused by obligate ectoparasitism, host specificity, and dependence on a specific environment that was rigorously selected by a very restricted number of host species. Host populations of univorous Laboulbeniales probably are similar to islands in the model of island biogeography.
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Species interactions can influence ecosystem functioning by enhancing or suppressing the activities of species that drive ecosystem processes, or by causing changes in biodiversity. However, one important class of species interactions - parasitism - has been little considered in biodiversity and ecosystem functioning (BD-EF) research. Parasites might increase or decrease ecosystem processes by reducing host abundance. Parasites could also increase trait diversity by suppressing dominant species or by increasing within-host trait diversity. These different mechanisms by which parasites might affect ecosystem function pose challenges in predicting their net effects. Nonetheless, given the ubiquity of parasites, we propose that parasite-host interactions should be incorporated into the BD-EF framework.
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Hippoboscid flies (Diptera: Hippoboscidae) include species that are ectoparasites of birds in the Northern Hemisphere, but little is known regarding their taxonomy, parasites, avian host associations, or geographical distribution in North America. In late August of 2013 and 2014, we collected hippoboscid flies from live birds trapped in mist nets as part of a banding study in Cypress Hills Interprovincial Park in southeastern Alberta, Canada. A total of 113 birds comprising 9 species was examined in 2013. Of these, 18 individuals were infested with 1-3 Ornithomya anchineuria Speiser (n = 22 flies; prevalence = 15.9%). Eight of these flies carried 1-8 adult female epidermoptid mites anchored to their ventral, posterior abdomens. Each female was associated with clusters of up to 30 stalked eggs. The first pair of tarsi on adult female mites were highly modified as anchors, indicating permanent attachment through the host cuticle. Morphological traits identified these mites as Myialges cf. borealis Mironov, Skirnisson, Thorarinsdottier and Nielsen. COI gene sequences obtained for 2 mites were distinct from those previously reported for species of Myialges, being most similar to Myialges trinotoni Cooreman. The paucity of available gene sequences for Myialges and related genera of epidermoptid mites prevents any further conclusions regarding taxonomy. These findings extend previous reports of O. anchineuria from Pacific and Atlantic coasts of Canada inland to the central migratory flyway of the Northern Great Plains, and expand the limited information available for Myialges spp.
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Arthropod-parasitic fungi of the order Laboulbeniales are known to exhibit specialization to individual host taxa in most cases. Some species exhibit ecological specificity to multiple, often unrelated hosts in certain microhabitats; and often position specificity to different host body parts. The myrmecophilous Rickia wasmannii (Ascomycota: Laboulbeniales) infects Myrmica species (Hymenoptera: Formicidae) (host specificity), and occasionally other arthropod inquilines inside the ant nest (ecological specificity). An effect of the position of infection on the thallus densities has also been reported. Another determinative factor that may also exist in the Rickia-Myrmica host-parasite system, the chronological age of ant worker hosts, has also been linked to parasite load. Comprehensive studies on the age-related infection intensity, however, are still lacking. Here we investigated whether the level of infection correlates with the age of the M. scabrinodis host consistently. We found that older hosts exhibited higher parasite load, even though the infection level of the different colonies varied widely. The results highlight that the level of R. wasmannii infections are strongly influenced by host individual and host colony factors.
Article
A first molecular-based phylogeny is presented for the Laboulbeniomycetes, a group of ascomycete fungi that utilize arthropods for nutrition and/or dispersal. Morphological diversification and life-history evolution has made it difficult to resolve relationships within the group, and to identify close relatives. Here, we infer a preliminary phylogeny based on acquisition of 51 new SSU rDNA sequences, representing a total of 65 taxa. The results of this study demonstrate that Laboulbeniomycetes is monophyletic, and related to Sordariomycetes. The class could be divided into at least four or five orders, though we refrain from formally giving names to these at this stage. Further evidence for the occurrence of asexuality within the class is provided by the inclusion of the genera Chantransiopsis and Tetrameronycha, both known only as asexual taxa with thalli consisting of linearly superposed cells. The precise placement of the genus Herpomyces (Herpomycetaceae), on cockroaches, remains unresolved in our analysis, but lies outside of the main clade of sexually reproducing Laboulbeniales. There is good support for this latter grouping, comprising taxa that are found on both aquatic and terrestrial hosts. Within this large assemblage, we recognize five distinct clades (clades E, F, G, H, I). Relationships among the so-called 'aquatic genera' (≡. Ceratomycetaceae + some Euceratomycetaceae) are poorly resolved in our analyses, accounting for three of these clades (E, F, G), with the remainder of the taxa (largely equivalent to Laboulbeniaceae) split into two major groupings (clades H, I). Across all taxa, antheridial characteristics, features on which the earliest classifications were based, are shown to be homoplastic. On the other hand, features of perithecial development show an overall trend towards reduction, and appear to be phylogenetically informative. Morphological characters are identified that support the dichotomy in the Laboulbeniaceae and subclades within the two major groupings are discussed further in light of information on thallus morphology, development, and host relationships.
Article
Laboulbeniales zijn obligaat ectoparasitaire schimmels (Ascomycota, Pezizomycotina) met Arthropoda als gastheren. Naar schatting zijn er 15.000 tot 75.000 soorten, waarvan er zo’n 2.100 beschreven zijn. Zeven soorten, in de geslachten Hesperomyces (6) en Laboulbenia (1), hebben lieveheersbeestjes (Coleoptera, Coccinellidae) als gastheer. Dit artikel geeft een korte bespreking van de biologie en ecologie van Laboulbeniales en de geschiedenis van het Laboulbeniales-onderzoek in Nederland. De verzamelde kennis wordt gegeven betreffende Hesperomyces virescens, een parasiet van lieveheersbeestjes die gekend is van 20 geslachten verdeeld over vijf subfamilies. De morfologie en de ecologie van deze schimmel worden besproken. Recent moleculair onderzoek toont aan dat deze schimmelsoort eigenlijk bestaat uit een aantal cryptische soorten die morfologisch nauwelijks of niet van elkaar te onderscheiden zijn. Deze cryptische soorten blijken echter gespecialiseerd te zijn op specifieke gastheersoorten. Op basis van de literatuur en originele data wordt een wereldwijd overzicht gegeven van het gastheerspectrum van het Hesperomyces virescens ‘soortencomplex’. Belangrijke inzichten betreffende de gastheerspecificiteit worden besproken en een stand van zaken betreffende Hesperomyces virescens en ‘hoofdgastheer’ Harmonia axyridis in Nederland wordt gegeven.
Conference Paper
Concluding remarks: Bat flies are highly specialized for a nearly permanent ectoparasitic relationship with their hosts, the Chiroptera. Although known life-histories are rather similar across all taxa, bat flies exhibit a variety of morphological adaptations, most suiting them for the two physical substrates offered to them by their bat hosts, the fur and the flight membranes. These morphological adaptations and the ecological diversity of their hosts make bat flies an excellent group in which to study the parasitic relationship, including morphological accommodations, cospeciation, and coevolution.
Article
Laboulbenia littoralis is described from the halobiont Cafius xantholoma (Coleoptera, Staphylinidae); it was previously misidentified and not properly documented. Morphologically the new species belongs to a group of carabidicolous taxa similar to Laboulbenia pedicellata and especially Laboulbenia slackensis. It is generally accepted that the specificity of Laboulbeniales is based on their specific need for substances from the host. In this relatively strict context, host shifts between unrelated hosts are difficult to explain. We present morphological and ecological evidence supporting the hypothesis that these fungi are capable of shifting between unrelated hosts, as long as they share the same habitat. Adaptation to a particular environment, combined with a reduced dependence from specific nutrients of the host, explains the proposed interfamilial host shift.