Project

Interactions between ants and Laboulbeniales fungi

Goal: A four-year-long Marie Curie CIG project, started in January 2013. See: http://web.unideb.hu/tartally/AntLab.htm
Up-to-date list of ant-Laboulbeniales papers: https://goo.gl/ueBHbL

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András Tartally
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Exploitation of organisms by multiple parasite species is common in nature, but interactions among parasites have rarely been studied. Myrmica ants are rich in parasites. Among others, the ectoparasitic Rickia wasmannii fungus and the socially parasitic caterpillars of myrmecophilous Phengaris butterflies often infect the same Myrmica colonies. In this study, we examined the effects of R. wasmannii on the adoption, long-term development, and survival of P. alcon . In laboratory conditions, caterpillars introduced into nests of Myrmica scabrinodis uninfected with R. wasmannii survived significantly longer compared to caterpillars introduced into infected nests. In the field, joint infection was less common than expected if both parasites exploited M. scabrinodis colonies independently. Pre-pupal caterpillars of P. alcon were somewhat larger in nests infected with R. wasmannii than those found in uninfected nests. Based on these results it seems that R. wasmannii infection of M. scabrinodis affects the survival and development of P. alcon caterpillars, suggesting competition between these two ant associates.
András Tartally
added a research item
Parasitism-generated negative effects on ant societies are multifaceted, implying individual and colony-level responses. Though laboratory based evidence shows that the sublethal fungus Rickia wasmannii is responsible for physiological and behavioral responses that may negatively affect individual workers’ resilience and life expectancy in Myrmica ant workers, colony-level stress response to this parasite is largely unknown. Here, we focus on understanding of a long-term, colony-level effect of Rickia infection on Myrmica scabrinodis ant populations by tracking trait size-based changes. We collected worker specimens from infected and uninfected colonies from the same population in order to: (1) compare body size in response to parasitism, (2) assess the extent to which possible changes in size are associated with the severity of infection, and (3) investigate shifts in body size in response to infection over time by testing correlation of workers’ ages and sizes. We found that workers from infected colonies were significantly smaller than their healthy congeners, but neither infection level nor the age of the workers showed significant correlation with the size in infected colonies. Decreasing body sizes in infected colonies can be ascribed to workers’ mediated effect toward developing larvae, which are unable to attain the average body size before they pupate.
András Tartally
added a research item
Laboulbeniales (Ascomycota: Laboulbeniomycetes) are obligate ectoparasitic fungi of arthropods with a worldwide distribution. Their effects on host physiology and behaviour as well as their ecology have recently gained wider attention. One aspect that is virtually unknown regarding Laboulbeniales and arthropod-associated fungi in general, is how abiotic factors shape the distribution of these parasites. We used ant- and bat fly-associated Laboulbeniales to study whether climatic elements play a role in the distribution of fungal species. We collected uninfected and Laboulbeniales-infected insects belonging to three species: bat flies Nycteribia schmidlii and Penicillidia conspicua (Diptera: Nycteribiidae) and the ant Myrmica scabrinodis (Hymenoptera: Formicidae). We used climatic variables and performed statistical analyses to explain the distribution of Laboulbeniales infection. Our results show a higher likelihood of Laboulbeniales presence in habitats with low annual mean temperature and humidity, suggesting that climatic elements can considerably shape the distribution of Laboulbeniales species.
Danny Haelewaters
added a research item
Fungal species identities are often based on morphological features, but current molecular phylogenetic and other approaches almost always lead to the discovery of multiple species in single morpho-species. According to the morphological species concept, the ant-parasitic fungus Rickia wasmannii (Ascomycota, Laboulbeniales) is a single species with pan-European distribution and a wide host range. Since its description, it has been reported from ten species of Myrmica (Hymenoptera, Formicidae), of which two belong to the rubra-group and the other eight to the phylogenetically distinct scabrinodis-group. We found evidence for R. wasmannii being a single phylogenetic species using sequence data from two loci. Apparently, the original morphological description (dating back to 1899) represents a single phylogenetic species. Furthermore, the biology and host-parasite interactions of R. wasmannii are not likely to be affected by genetic divergence among different populations of the fungus, implying comparability among studies conducted on members of different ant populations. We found no differences in total thallus number on workers between Myrmica species, but we did observe differences in the pattern of thallus distribution over the body. The locus of infection is the frontal side of the head in Myrmica rubra and M. sabuleti whereas in M. scabrinodis the locus of infection differs between worker ants from Hungary (gaster tergites) and the Netherlands (frontal head). Possible explanations for these observations are differences among host species and among populations of the same species in (i) how ant workers come into contact with the fungus, (ii) grooming efficacy, and (iii) cuticle surface characteristics. © D. Haelewaters et al., published by EDP Sciences, 2019.
Ferenc Báthori
added a research item
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.
Ferenc Báthori
added a research item
Public awareness has been raised on the importance of natural history and academic collections for science and society in a time when reduced financial support and staff cuts are prevalent. In the field of biology, new species and new interspecies associations are constantly discovered by making use of museum collections, digitalised materials or citizen science programs. In our study, the Myrmica Latreille, 1804 image collection of AntWeb.org was screened for fungal ectoparasites. A total of 397 imaged specimens from 133 species were visually investigated. A single specimen of M. hellenica Finzi, 1926, collected in Greece by U. Sahlberg, showed a conspicuous fungal infection. The parasite was identified using microscopic methods as Rickia wasmannii Cavara, an ectoparasitic fungal species specialised to Myrmica ants. This finding represents a new country record and a new Myrmica species for the host spectrum of R. wasmannii. According to our results, online entomological databases can be screened relatively easily for ectoparasitic fungal infections from new hosts and new regions. However, depending on quality of the insect voucher photos, additional investigation of the material could be needed to confirm the identity of the parasite.
Ferenc Báthori
added a research item
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.
András Tartally
added 2 research items
The first records of Rickia wasmannii CAVARA, 1899, a myrmecophilous fungus, and its Myrmica LATREILLE, 1804 host ants in Hungary and Romania (Ascomycetes: Myrmecol. News 10: 123 Rickia wasmannii CAVARA, 1899 (Ascomycetes: Laboul-beniales) obligately exploits ants (for a review on Laboul-beniales: WEIR & BLACKWELL 2005; and for one espe-cially on myrmecophilous species: HERRAIZ & ESPADALER 2007). The ants appear to be neutral to the presence of this fungus on their cuticules (A. Tartally, pers. obs.). Myrmica LATREILLE, 1804 (Hymenoptera: Formicidae) species are reported to be the usual hosts of R. wasmannii (HERRAIZ & ESPADALER 2007). To the best of our knowledge, this fungus has not been reported previously from the Carpa-thian Basin. The occurrence of R. wasmannii was checked on 5788 Myrmica specimens from 580 colonies collected between 2001 and 2006 at 26 sites in Hungary and three sites in Transylvania, Romania (Fig. 1), and the density of the fungus on the different parts of the body of infected Myrmica specimens was estimated. The fungus was pres-ent on 353 infected ant specimens in 45 colonies at nine Hungarian and two Transylvanian sites (Fig. were involved in our work, only four of them (M. salina, M. scabrinodis, M. specioides and M. vandeli) were found to be infected. M. scabrinodis was the most common host, and M. salina was most heavily infected. The fungus was present on workers (Figs. 2 -4) and dealate (old) queens, but not on males, alate (young) queens and larvae. How-ever, the numbers of males, alate queens and larvae exam-ined were small. Our results indicate that it is quite prob-able that R. wasmannii could be found at several other sites in the Carpathian Basin with a more intensive survey.
Abstract: Laboulbenia formicarum Thaxt. (Ascomycota: Laboulbeniales) fungus is native to N-America and has just been recorded from Europe from the invasive ant Lasius neglectus van Loon, Boomsma et Andrásfalvy, 1990 (Hymenoptera: Formicidae). The ant is well known from Hungary but the fungus is not known from there. We checked the infection of L. formicarum at the Hungarian L. neglectus localities and had negative results.
András Tartally
added 3 research items
Among the many associations between fungi and ants, the associations involving the ectoparasitic fungi Laboulbeniales (Ascomycota: Laboulbeniales) have remained largely enigmatic even today. However, for two of the six ant-parasitizing Laboulbeniales, it has been found that parasitism is correlated with diminished survival of their hosts, especially under resource limitation. In the present study, we investigate whether these fitness impacts are linked to an intrusion into the body cavity by the ectoparasites. Light, scanning and transmission electron microscopy were used to study the mode of attachment and the presence of penetrating structures in four of the six currently recognized ant-parasitizing Laboulbeniales. No indication of penetration was found, suggesting that the reported fitness impacts are not linked to an intrusion into the body cavity. A better understanding of host-parasite interactions involving Laboulbeniales on ant hosts is necessary, considering that Laboulbeniales parasitizing ants impact their hosts' fitness and that monitoring studies have revealed that an infection with Laboulbeniales is much more common in European ants than previously thought.
András Tartally
added 2 research items
Tartally, A. (2000): Notes on the coexistence of the supercolonial Lasius neglectus van Loon, Boomsma et Andrásfalvy 1990 (Hymenoptera: Formicidae) with other ant species. — Tiscia 32, 43-46. Abstract. Lasius neglectus is an invasive species known for about ten years. This species excludes other ant species from the areas of its supercolonies and causes much trouble for people by intruding to their houses. Apart from these, there is not much we know about the ecology of L. neglectus. The aim of my paper is to compare ant communities living in the border and in the centre of the L. neglectus colonies. As my experiences show L. neglectus reaches a quite high abundance in the centres of the supercolonies at the expense of the abundance of other ant species. It was proved using the χ 2 test, that the distribution of the L. neglectus in the centre area and the border was significantly different (p<0.95). We have also demonstrated that the Shannon diversity of the centre assemblage is significantly smaller than the diversity of the border (p<0.95). This can be explained by the polygynous strategy, which is characteristic for Lasius neglectus.
András Tartally
added 6 research items
The order Laboulbeniales comprises more than 2000 species in about 140 genera (Santamaria, 2001; Weir & Black-well, 2005; Kirk et al., 2008). They are obligate ectoparasites of arthropods, and approximately 80% of the described Laboulbe-niales species parasitize Coleoptera species (Santamaria, 2001; Henk et al., 2003; Weir & Blackwell, 2005). In the order Hymenoptera, only ants are known to be hosts of certain species of Laboulbeniales (Espadaler & Santamaria, 2003). Thus far, four species of these fungi have been reported to be associated with ants in Europe: Rickia wasmannii Cavara, 1899, is found in 15 countries on eight Myr-mica species; Laboulbenia formicarium Thaxt, 1908, in France, Portugal and Spain on two Lasius species; Laboulbenia camponoti Batra, 1963, in Bulgaria and Spain on five Camponotus spe-cies; and Rickia lenoirii Santamaria and Espadaler, 2014, in Greece and France on two Messor species (Herraiz & Espadal-er, 2007; Lapeva-Gjonova & Santamaria, 2011; Espadaler & Santamaria, 2012; Santamaria & Espadaler, 2014). The effect of these ant parasitic fungi on their hosts is rather understudied except for the work of Csata et al. (2014). Abstract Laboulbenia camponoti Batra, 1963 (Ascomycota: Laboulbeniales), has been found on Camponotus aethiops (Latreille, 1798) (Hymenoptera: Formicidae) workers in the Carpathian Basin: in Baziaş, Caraş-Severin (Romania), and Vien-na (Austria). Vienna is the northernmost known locality of this fungus (48°12' N). These new observations expand the area of L. camponoti from regions with Mediterranean and subtropical climatic influences to the common borders of the Continental and Pannonian regions. These results show that Camponotus samples from other climatic regions should be examined more closely for this fungal parasite.
The order Laboulbeniales (Fungi, Ascomycota) is a little-studied group of microscopic ectoparasites of invertebrates, mostly insects. The effects of Laboulbeniales species on their hosts are mostly unknown. Rickia wasmannii Cavara, 1899 is a common Laboulbeniales fungus occurring in Europe and is currently known to be a parasite of at least eight Myrmica ant species. Rickia wasmannii serves as a good model organism for Laboulbeniales-host interactions, as this species covers the host in a very high density, and infected host individuals can be easily collected in high numbers. The effect of R. wasmannii on the survival rate of its most common host species, Myrmica scabrinodis Nylander 1846, was therefore investigated in a laboratory experiment on an individual level. To enhance the results, environmental stresses were simulated by depriving infected and uninfected workers of water and food. The survival of individuals was recorded hourly until the death of the last individual. Infected specimens were significantly more sensitive to the withdrawal of food and water than uninfected specimens. When we tested for water consumption, we found that infected ants spent more time consuming water than uninfected ants. Therefore, it is possible that infected ants must replace the loss of water. Based on these results, R. wasmannii substantially decreases the chances and time of survival of infected individuals, at least in resource-limited environments, which suggest that R. wasmannii has a negative effect on its host. Copyright © 2015. Published by Elsevier Inc.
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.
Danny Haelewaters
added a research item
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. © W.P. Pfliegler et al., published by EDP Sciences, 2016.
András Tartally
added a project goal
A four-year-long Marie Curie CIG project, started in January 2013. See: http://web.unideb.hu/tartally/AntLab.htm
Up-to-date list of ant-Laboulbeniales papers: https://goo.gl/ueBHbL