Danny Haelewaters

The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is native to Asia but has been intentionally introduced to many countries as a biological control agent of pest insects. In numerous countries, however, it has been introduced unintentionally. The dramatic spread of H. axyridis within many countries has been met with considerable trepidation. It is a generalist top predator, able to thrive in many habitats and across wide climatic conditions. It poses a threat to biodiversity, particularly aphidophagous insects, through competition and predation, and in many countries adverse effects have been reported on other species, particularly coccinellids. However, the patterns are not consistent around the world and seem to be affected by many factors including landscape and climate. Research on H. axyridis has provided detailed insights into invasion biology from broad patterns and processes to approaches in surveillance and monitoring. An impressive number of studies on this alien species have provided mechanistic evidence alongside models explaining large-scale patterns and processes. The involvement of citizens in monitoring this species in a number of countries around the world is inspiring and has provided data on scales that would be otherwise unachievable. Harmonia axyridis has successfully been used as a model invasive alien species and has been the inspiration for global collaborations at various scales. There is considerable scope to expand the research and associated collaborations, particularly to increase the breadth of parallel studies conducted in the native and invaded regions. Indeed a qualitative comparison of biological traits across the native and invaded range suggests that there are differences which ultimately could influence the population dynamics of this invader. Here we provide an overview of the invasion history and ecology of H. axyridis globally with consideration of future research perspectives. We reflect broadly on the contributions of such research to our understanding of invasion biology while also informing policy and people.

Laboulbenia slackensis and L. littoralis sp. nov. (Ascomycota, Laboulbeniales), two sibling species as a result of ecological speciation

Laboulbenia littoralis is described from the halobiont Cafius xantholoma (Coleoptera, Staphylinidae); it previously was 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 need for substances from the host. In this relatively strict context, 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.

Laboulbeniales (Ascomycota) of the Boston Harbor Islands I: species parasitizing Coccinellidae and Staphylinidae, with comments on typification.

Abstract This paper, based on a recent comprehensive sampling of insects, is the first report of Laboulbeniales from the New England region since the 1930s. We present 7 new records of laboulbenialean parasites on Staphylinidae (rove beetles) and Coccinellidae (lady beetles) from the Boston Harbor Islands National Recreation Area. These are Clonophoromyces nipponicus Terada & I.I. Tav., Hesperomyces virescens Thaxt., Ilyomyces cf. mairei F. Picard, Laboulbenia philonthi Thaxt., Peyritschiella protea Thaxt., Stichomyces conosomatis Thaxt., and Teratomyces actobii Thaxt. One of these parasite species, C. nipponicus, has not been found previously outside of its type locality in Japan. Examination of Roland Thaxters 1891–1932 slides led to the designation of lectotypes for L. philonthi, P. protea, S. conosomatis, and T. actobii. The following synonymy is established: Teratomyces brevicaulis Thaxt. = T. actobii. In addition, we discovered new localities for H. virescens (from Canada, Cuba, Guatemala, and Japan) and L. philonthi (from Canada, Grenada, Panama, Trinidad, and Venezuela).

Bringing Laboulbeniales into the 21st century: enhanced techniques for extraction and PCR amplification of DNA from minute ectoparasitic fungi

Laboulbeniales is one of the most peculiar orders of Ascomycota. These fungi are characterized by an ectoparasitic life-style on arthropods, determinate growth, lack of an asexual stage, high species richness, and intractability to culture. The order Laboulbeniales, sister to Pyxidiophorales, has only recently been assigned a separate class, the Laboulbeniomycetes, based on very few ribosomal DNA sequences. So far, DNA isolations and PCR amplifications have proven difficult. Here, we provide details of isolation techniques and the application of commercially available kits that enable efficient and reliable genetic analyses of these fungi. We provide 43 newly generated Laboulbeniales ribosomal DNA sequences, among which are the first published sequences for species in the genera Gloeandromyces, Herpomyces, Laboulbenia, Monoicomyces, and Polyandromyces. DNA extractions were possible using from 1 to 30 thalli from hosts preserved in ethanol (70–100 %). In two cases, we successfully isolated DNA from thalli on dried insect collections. Laboulbeniales molecular systematics could be substantially enhanced through these improved methods by allowing more complete sampling of both taxa and gene regions.

Studies of Laboulbeniales (Fungi, Ascomycota) on Myrmica ants: Rickia wasmannii in the Netherlands

An important group of fungal insect parasites is the Laboulbeniales (Ascomycota). These are microscopic in size and live attached to the cuticle of their arthropod hosts. Rickia wasmannii is a common European species limited to the ant genus Myrmica (Hymenoptera, Formicidae). We present new records of R. wasmannii in the Netherlands on three host species: Myrmica ruginodis, M. sabuleti, and M. scabrinodis. Our data show a mass infection of M. sabuleti by R. wasmannii. The average parasite prevalence is 38% (n = 3,876). The prevalence was much lower on the other Myrmica species. So far, R. wasmannii infections have been found only on Myrmica species in the rubra-group and the scabrinodis-group. We provide possible explanations for this observation. To date, Rickia wasmannii is known on nine Myrmica species in sixteen European countries; an overview is included in tabulated form.

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.

Studies of Laboulbeniales on Myrmica ants (III): myrmecophilous arthropods as alternative hosts of Rickia wasmannii

Myrmecophilous arthropods and their manifold relations to host ants are interesting from an evolutionary perspective. Rickia wasmannii is an ectoparasitic fungus belonging to the Laboulbeniales order. Here, we show that inquiline mites can become infected by R. wasmannii, which was thought to be restricted to the genus Myrmica (Hymenoptera: Formicidae). This is the first report of R. wasmannii from an alternative host in another subphylum (Chelicerata). We also found immature fruiting bodies on a larva of Microdon myrmicae (Diptera: Syrphidae), which represents the first report of any Rickia species on flies. This fungus is capable of infecting alternative, unrelated host species as they co-occur in the ant nest “microhabitat”. These observations provide direct evidence for ecological specificity in Laboulbeniales. The presence of R. wasmannii on inquilines in Myrmica ant nests suggests that the parasite may have adapted to the ant nest environment and is less dependent on acquiring specific nutrients from the hosts. However, the alternative cannot be excluded; these infections might also represent chance events if the fungus is incapable of fulfilling its life cycle.

Hesperomyces virescens (Fungi, Ascomycota, Laboulbeniales) attacking Harmonia axyridis (Coleoptera, Coccinellidae) in its native range

This study intended to find data on obligate ectoparasitic Laboulbeniales (Fungi, Ascomycota) on Chinese Harmonia axyridis (Coleoptera, Coccinellidae). After having screened over four thousand dried specimens of H. axyridis and close relatives, we present the first (historical) record of Chinese H. axyridis infected with Hesperomyces virescens. We suggest that H. virescens is a historically globally distributed species and hypothesize that (native) infection was lost when H. axyridis was introduced in North America.

Studies of laboulbeniales (Fungi, Ascomycota) on myrmica ants (II) : Variation of infection by Rickia wasmannii over habitats and time

One group of important insect parasites are the Laboulbeniales (Ascomycota), microscopic fungi that live attached to the exterior of their hosts, mainly beetles, but also mites, millipedes, earwigs, and ants. Rickia wasmannii is a common fungus in Europe and is limited to the ant genus Myrmica (Hymenoptera, Formicidae). This paper presents patterns of R. wasmannii infection in the Netherlands from three host species collected in three series of pitfall traps: Myrmica ruginodis, M. sabuleti, and M. scabrinodis. The infection rate of especially M. sabuleti was so high, that it allowed analyses of infection patterns over time and habitats. We found that only workers were infected, mostly the older ones with a hard cuticle. Gynes are probably never infected. This is supported with data from a nature restoration site: in this young area R. wassmannii is not abundant in contrast to close-by sites, so there probably is a build-up of infection by Rickia over time through worker contact. Taken over three periods throughout the year (spring, summer, autumn), parasite prevalence declined significantly in M. sabuleti, with a non-significant declining trend in M. scabrinodis. Increased allogrooming behavior in the nest in the winter may be the main contributing factor for this. New, largely uninfected cohorts of workers lead to decreased infection rate during the reproduction season. Finally, Rickia wasmannii occurs throughout a wide variety of habitats, from moist and cool to dry and warm.

Three new species of Laboulbenia from Roland Thaxter’s backlog of slides and a brief review of Laboulbeniales associated with Chrysomelidae

Three new species of Laboulbenia parasitic on Chrysomelidae are described from material mounted by Roland Thaxter (1858–1932). These are L. bilobata on Lema spp. from Brazil and Trinidad; L. longipilis from Cameroon; and L. pfisteri on Ivongius sp. from Madagascar. The following species of Laboulbenia on Chrysomelidae are illustrated for the first time: L. macarthurii, L. minuscula, L. nodostomatis, L. obesa, and L. philippina, all of which were described by Thaxter in 1914. A list of all 69 described Laboulbeniales associated with Chrysomelidae is presented in tabulated form.