Laboulbeniales Fungi Research Articles

Hyperparasitism in bat flies (Diptera: Streblidae): new records and interaction networks in the Neotropics

Hyperparasitism is defined as the interaction where one parasite is infected by another parasite. In bat flies (Streblidae and Nycteribiidae), both hyperparasites and microparasites (bacteria, viruses, fungi, and arthropods such as mites) have been documented. Fungi belonging to the order Laboulbeniales are microscopic parasites of a wide diversity of arthropod hosts. Three genera exclusively target bat flies: Arthrorhynchus, which parasitizes species within Nycteribiidae in the Eastern Hemisphere, while genus Gloeandromyces and Nycteromyces parasitize Streblidae in the Western Hemisphere. Among the hyperparasitic arthropods, mites of family Neothrombidiidae, particularly the monospecific genus Monunguis, are known to parasitize bat flies. Here we present the first records of the hyperparasites Monunguis streblida and Gloeandromyces pageanus f. polymorphus parasitizing Streblidae bat flies in Colombia and a summary of these hyperparasitic interactions in the Neotropics. We detected fungi and mites parasitizing bat flies that were collected in the Magdalena River Basin, Colombia, in field expeditions in 2018, 2022, and 2023. We identified 17 bat flies and two species of hyperparasites, specifically M. streblida and the fungi Gloeandromyces. Our search for reports of these interactions in the Neotropics revealed that seven species of Trichobius (Streblidae) are parasitized by M. streblida, whereas Paratrichobius longicrus (Streblidae) is parasitized by Gloeandromyces pageanus f. polymorphus. These interactions have been reported in 11 countries, but our records are the first of M. streblida and Laboulbeniales fungi parasitizing bat flies in Colombia. So far, a total of 14 species of fungi and one species of mite have been associated with 19 species of bat flies, which in turn, are linked to 15 species of Neotropical bats.

Species of Laboulbeniales fungi parasitic on some common Indian insects: Isolation, visualization and characterization by Scanning Electron Micrographs (SEM)

The Laboulbeniales are a group of lesser-known fungi. They occur as ectoparasites on the exoskeleton of various arthropod species, mainly beetles, cockroaches, ants, dipterans and a few millipede genera appearing as hairs/bristles coming out of their cuticle. They are small, non-mycelial fungi forming compact multicellular thalli, starting from a two-celled sheathed ascospore which continues to envelop the mature thallus. The fungi, being obligate, spend their entire life cycle on their insect hosts. The present study attempted to locate the Laboulbeniales fungi in the common insects of India, isolate them and identify them based on morphology. Different species of insects; Carabid beetles - Stenolophus sp., Bembidion sp., Black ants - Camponotus sp., and Earwigs - Labidura riparia; were collected from different habitats of damp garden soil, river banks, light sources and entomological collection museum situated as different sites New Delhi. The insects were scrutinized for the presence of fungi through light and scanning electron microscopy. The morphological features of each fungus were recorded, and the species were characterized. The studies showed the presence of Laboulbenia anaplogenii and L. stenolophi on the legs of Stenolophus sp.; L. egens on Bembidion sp. legs; L. camponoti on the wings of black ants and Dimeromyces anisolabis on the legs of earwigs. The identification was made primarily based on the size, shape and structure of basal foot, receptacles, antheridia and foot of the thallus or it’s remnant scar found on the insect cuticle. This is the first Indian report of conducting scanning imaging of the Laboulbeniales fungi.

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

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.

Insects and their Laboulbeniales (Ascomycota, Fungi) of Lake Eustis and Emeralda Marsh Conservation Area: A case study on urbanization and diversity.

A rapid biodiversity assessment of insects and associated Laboulbeniales fungi was conducted over the course of five nights in August, 2018, at two central Florida lakes: Lake Eustis and the nearby protected and restored National Natural Landmark, Emeralda Marsh Conservation Area (EMCA), which encompasses a portion of Lake Griffin. Lake Eustis was surveyed for Laboulbeniales in 1897 by mycologist Dr. Roland Thaxter but has not since been investigated. Because Lake Eustis has been urbanized, with the lake perimeter almost entirely altered by human development, the site offers a look into Laboulbeniales diversity across a 121‐year timeline, before and after human development. By surveying Lake Eustis and EMCA, a modern case study comparison of Laboulbeniales and insect diversity between a developed and a protected and restored system is made. A total of 4022 insects were collected during the rapid assessment. Overall, insect abundance was greater at EMCA, with 3001 insects collected, than 1021 insects collected from Eustis. Although family‐level insect richness was comparable between sites, with 55 families present at EMCA and 56 at Eustis, 529 out of 3001 (17.6%) of the insects collected at EMCA were hosts to parasitic Laboulbeniales fungi, whereas only 2 out of 1021 (0.19%) collected from Eustis were infected. A total of 16 species of Laboulbeniales found at EMCA compared with only one at Eustis. The current number of Laboulbeniales species documented at Eustis was incredibly depauperate compared with the 26 species and two varieties recorded by Thaxter in 1897. These findings suggest the possibility of utilizing Laboulbeniales as indicators of ecosystem health, and future research should investigate this question further. A figure displaying host–parasite records and a species list of Laboulbeniales are presented. Finally, updated occurrence records for species of Ceratomyces and Hydrophilomyces are provided.

Penetrative and non-penetrative interaction between Laboulbeniales fungi and their arthropod hosts

Laboulbeniales are a highly specialized group of fungi living only on arthropods. They have high host specificity and spend their entire life-cycle on an arthropod host. Taxonomic characters of Laboulbeniales are based on the architecture of the cells of the parenchymal thallus, i.e. the visible part of the fungus outside the host. The extent of the fungus spreading inside the host—the haustorium—remains largely unknown. The attachment to the arthropod host is fundamental to understand the fungus-animal interaction, but how this truly occurs is unclear. Recent evidences question the strictly parasitic life-style of Laboulbeniales. We used micro-computed tomography (µCT) and 3D reconstructions to visualize, for the first time, the complete structure of Laboulbeniales species in situ on their hosts. We compared the haustoriate species, Arthrorhynchus nycteribiae on an insect host to the non-haustoriate species, Rickia gigas on a millipede host. Our results confirm that some Laboulbeniales species are ectoparasitic and have a haustorial structure that penetrates the host’s cuticle, while others are ectobionts and are only firmly attached to the host’s cuticle without penetrating it. The presence and the morphology of the haustorium are important traits for Laboulbeniales evolution, and key factors for future understanding of host dependence and specificity.

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

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.

Effects of fungal infection on the survival of parasitic bat flies

BackgroundParasites are able to alter numerous aspects of their hosts’ life history, behaviour and distribution. One central question in parasitology is to determine the degree of impact that parasites have on their hosts. Laboulbeniales (Fungi: Ascomycota) are ectoparasitic fungi of arthropods. Even though these fungi are widely distributed, little is known about their ecology and their possible physiological effects on their hosts. We used a highly specific bat fly-fungi association to assess the effect of these fungal parasites on their dipteran hosts.MethodsWe collected bat flies (Diptera: Nycteribiidae) belonging to two species, Nycteribia schmidlii and Penicillidia conspicua from their bat host Miniopterus schreibersii (Chiroptera: Miniopteridae). We experimentally tested the effect of infection on the lifespan of bat flies.ResultsThe prevalence of Laboulbeniales fungi was 17.9% in N. schmidlii and 64.8% in P. conspicua. Two fungi species were identified, Arthrorhynchus eucampsipodae and A. nycteribiae, both showing strict host specificity with N. schmidlii and P. conspicua, respectively. We found that fungal infection reduced by half the survival rate of P. conspicua regardless of sex, whereas N. schmidlii was not affected by the infection. Moreover, the intensity of infection showed negative correlation with the lifespan of P. conspicua.ConclusionsTo our knowledge, this is the first indication that fungal infection can alter bat fly survival and thus may play a significant role in the population dynamics of these bat ectoparasites.

The place of Carabidae in the biosphere – a network approach

Whereas they are of high ecological, conservation, and agricultural importance, ground beetles (Coleoptera: Carabidae) are amongst the organisms declining rapidly as a result of human activities. Since they are part of a complex ecological network –in which other taxa’s survival may depend on them, or they may depend on other taxa –in the case of their, hypothetical, extinction these connections would be impaired. In order to gain insight how different taxa would be affected by the extinction of carabids, and thus, how ecosystem functions would be altered, we conceptualised a network between ground beetles and all other organisms they are directly connected with. We used published literature data in building our network, thus interaction occurrences are likely to be skewed by research interest. Based on a single database search, we found 238 carabid species interacting with 395 other species, including plants (72), fungi (53), animals (286), and 7 other Eucaryota. Of the 817 described interactions, in 235 cases, carabids were prey, mostly for birds and mammals. Hosting ectoparasites was the second most frequent relationship, with 144 connections. Most of these connections were to Laboulbeniales fungi. Further, detailed searches on carabid – fungus relationshipsyielded over 700 different interactions. Carabids were listed to consume 88 other taxa, including many plants; an additional 200 records refer to seed predation by ground beetles, mostly from the Zabrini and Harpalini tribes. The specificity of seed dispersal, and therefore assessing the extent plant species depend on carabids was not possiblefrom this database. Carabids also visit flowers and even pollinate them in 12 cases. Amara, Harpalus and Cicindela genera had the most records of interactions with other species. Although this list of interactions between Carabidae and other taxa is incomplete, it shows that many other organisms can depend on ground beetles, and some (mostly fungi) have specific relationship with them. The apparent information gaps on symbiotic and competitive interactions, and the geographical bias towards Europe and North America open doors for further research in these areas.

Laboulbeniales (Fungi: Ascomycota) infection of bat flies (Diptera: Nycteribiidae) from Miniopterus schreibersii across Europe

BackgroundBat 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.ResultsSix 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.ConclusionsWith 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.

Host age determines parasite load of Laboulbeniales fungi infecting ants: Implications for host-parasite relationship and fungal life history

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.

A tripartite survey of hyperparasitic fungi associated with ectoparasitic flies on bats (Mammalia: Chiroptera) in a neotropical cloud forest in Panama.

The Darién province in eastern Panama is one of the most unexplored and biodiverse regions in the world. The Chucantí Nature Reserve, in Serranía de Majé, consists of a diverse tropical cloud forest ecosystem. The aim of this research was to explore and study host associations of a tripartite system of bats, ectoparasitic flies on bats (Diptera, Streblidae), and ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies as hosts. We captured bats at Chucantí, screened each bat for presence of bat flies, and screened collected bat flies for presence of Laboulbeniales. We mistnetted for 68 mistnet hours and captured 227 bats representing 17 species. We captured Micronycteris schmidtorum, a species previously unreported in Darién. In addition, we encountered the rarely collected Platyrrhinus dorsalis, representing the westernmost report for this species. Of all captured bats, 148 carried bat flies (65%). The number of sampled bat flies was 437, representing 16 species. One species represents a new country record (Trichobius anducei) and five species represent first reports for Darién (Basilia anceps, Anatrichobius scorzai, Nycterophilia parnelli, T. johnsonae, T. parasiticus). All 74 bat fly species currently reported in Panama are presented in tabulated form. Of all screened bat flies, 30 bore Laboulbeniales fungi (7%). Based on both morphology and large ribosomal subunit (LSU) sequence data, we delimited 7 species of Laboulbeniales: Gloeandromyces nycteribiidarum (newly reported for Panama), G. pageanus, G. streblae, Nycteromyces streblidinus, and 3 undescribed species. Of the 30 infected flies, 21 were Trichobius joblingi. This species was the only host on which we observed double infections of Laboulbeniales.

The effect of Rickia wasmannii (Ascomycota, Laboulbeniales) on the aggression and boldness of Myrmica scabrinodis (Hymenoptera, Formicidae)

The interactions of ectosymbiotic Laboulbeniales (Ascomycota) fungi and their hosts are rather understudied. Rickia wasmannii Cavara is a common ant-associated Laboulbeniales species that has been reported in 17 countries of Europe, and frequently infects Myrmica scabrinodis Nylander, 1846 (Hymenoptera: Formicidae), a common ant species host, in high density. These make M. scabrinodis and R. wasmannii appropriate model organisms for studies on fungal host-ectosymbiont interactions. Aggressiveness and boldness of infected and uninfected M. scabrinodis workers from northern and eastern Hungary were studied in two laboratory-established behavioural experiments. Infected workers were significantly less aggressive and less bold (i.e. less likely to leave nest shelters) than the uninfected ones. These results suggest that R. wasmannii has considerable effects on the behaviour of M. scabrinodis. Our study brings an evidence that infection of ants with Laboulbeniales might negatively affect the workers’ behaviour. In special, the competitive abilities might be affected most by these fungi, since remaining inside and behaving submissively is not effective behaviour in the case of significant competition for resources among colonies.

A "clean" alien species? Parasites of the invasive ladybird Harmonia axyridis (Coleoptera: Coccinellidae)

The multicoloured Asian ladybird Harmonia axyridis is an invasive insect that can negatively influence biodiversity and human economy in invaded areas. According to the enemy release hypothesis, invasive alien species are often little affected by parasites and other enemies. We studied the prevalence of common parasites of insects infesting and infecting H. axyridis in NW Poland. A large sample of 2351 individuals was collected and divided into two groups: 1180 beetles were dissected and examined for the presence of eugregarines, nematodes and Laboulbeniales fungi, and 751 were checked for phoretic mites. Our results show that H. axyridis is indeed parasitized infrequently. The prevalence of eugregarines and nematodes was very low (1.5% and 0.4%, respectively). No specimens of Laboulbeniales or phoretic mites were found. Our study indicates that in NW Poland H. axyridis is rarely infested or infected by parasites. This paper reports for the first time the infection of H. axyridis by the eugregarine Gregarina barbarara.

Parasites of parasites of bats: Laboulbeniales (Fungi: Ascomycota) on bat flies (Diptera: Nycteribiidae) in central Europe

BackgroundBat 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).ResultsWe 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.ConclusionsWe 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.

First Records Of The Recently Described Ectoparasitic Rickia lenoirii Santam. (Ascomycota: Laboulbeniales) In The Carpathian Basin

Rickia lenoirii has been reported in seven localities in the Carpathian Basin, six in Hungary and one in Romania, on Messor structor (Hymenoptera: Formicidae) host specimens. This is the first occurrence of this fungus in two new (Pannonian and Continental) biogeographic regions. According to our findings, the northernmost (47°31'33.01N) known occurrence of R. lenoirii is Ferenc-hegy (Ferenc Hill) in Budapest. These results demonstrate that ant-parasitic Laboulbeniales fungi may have wider distribution areas than previously expected by mycologists and myrmecologists.

Is sexually transmitted fungal infection evidence for size-related mating success in Neotropical guava fruit flies?

Se estudió poblaciones naturales de la mosca frutera Anastrepha striata Schiner, en dos lugares de Costa Rica. Los hongos Laboulbeniales se transmiten en éstas durante la cópula. Hembras y machos con hongos en las patas y/o parte ventral del tórax (machos), y en ambos lados del noto y/o base dorsal del abdomen (hembras), teRÍan alas significativamente más largas que los individuos no parasitados. Esto sugiere que los individuos más grandes logran más apareamientos.