Rickia Wasmannii Research Articles

Infection with a non-lethal fungal parasite is associated with increased immune investment in the ant Myrmica scabrinodis

Social insects, such as ants, are preferred host organisms of pathogens and parasites because colonies are densely populated, and the number of potential hosts is high in the same place and time. Within a colony, individuals are exposed differentially to risks according to their function and age. Thus, older individuals forage and are therefore the most exposed to infection, predation, or physical stress, while young workers mostly stay inside the sheltered nest being less exposed. Immune investment is considered to be dependent on an individual’s age and pathogen pressure. Long-term exposure to a parasite could affect the immune activity of individuals in an intriguing way that interferes with the age-dependent decline in immunocompetence. However, there are only few cases in which such interferences can be studied. The myrmecopathogenic fungus Rickia wasmannii, which infects entire colonies without killing the workers, is a suitable candidate for such studies. We investigated the general immunocompetence of Myrmica scabrinodis ant workers associated with non-lethal fungal infection by measuring the levels of active phenoloxidase (PO) and total PO (PPO) (reflecting the amount of both active and inactive forms of the enzyme) in two age classes. The level of PO proved to be higher in infected workers than in uninfected ones, while the level of PPO increased with age but was not affected by infection. Overall, these results indicate that a long-term infection could go hand in hand with increased immune activity of ant workers, conferring them higher level of protection.

Non-lethal fungal infection could reduce aggression towards strangers in ants

Many parasites interfere with the behaviour of their hosts. In social animals, such as ants, parasitic interference can cause changes on the level of the individual and also on the level of the society. The ant-parasitic fungus Rickia wasmannii influences the behaviour of Myrmica ants by expanding the host’s nestmate recognition template, thereby increasing the chance of the colony accepting infected non-nestmates. Infected ants consistently show an increase of the alkane tricosane (n-C23) in their cuticular hydrocarbon profiles. Although experimental application of single compounds often elicits aggression towards manipulated ants, we hypothesized that the increase of n-C23 might underlie the facilitated acceptance of infected non-nestmates. To test this, we mimicked fungal infection in M. scabrinodis by applying synthetic n-C23 to fresh ant corpses and observed the reaction of infected and uninfected workers to control and manipulated corpses. Infected ants appeared to be more peaceful towards infected but not uninfected non-nestmates. Adding n-C23 to uninfected corpses resulted in reduced aggression in uninfected ants. This supports the hypothesis that n-C23 acts as a ‘pacifying’ signal. Our study indicates that parasitic interference with the nestmate discrimination of host ants might eventually change colony structure by increasing genetic heterogeneity in infected colonies.

Ectoparasitic fungi of Myrmica ants alter the success of parasitic butterflies

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 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 parasites.

Ectoparasitic fungi Rickia wasmannii infection is associated with smaller body size in Myrmica ants

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.

Studies of Laboulbeniales on Myrmica ants (IV): host-related diversity and thallus distribution patterns of Rickia wasmannii.

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.

Infection-related variation in cuticle thickness in the ant Myrmica scabrinodis (Hymenoptera: Formicidae)

Cuticle quality is of vital importance in insects. It prevents desiccation, provides mechanical strength and protects against pathogens. The within-species variation of cuticular structure is affected by many factors. We investigated the relationship of the presence/absence of the ectoparasitic fungus Rickia wasmannii and cuticle thickness of its ant host Myrmica scabrinodis. Infected ants had thinner cuticle than uninfected ones, while there were also differences among populations. It is unclear whether reduced thickness is the host’s response, or whether the fungus infects preferentially colonies with ants that have a thin cuticle. Either way, within-species variation is linked to the presence of an epicuticular parasite.

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.

Online image databases as multi-purpose resources: discovery of a new host ant of Rickia wasmannii Cavara (Ascomycota, Laboulbeniales) by screening AntWeb.org

Online image databases as multi-purpose resources: discovery of a new host ant of Rickia wasmannii Cavara (Ascomycota, Laboulbeniales) by screening AntWeb.org

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.

Lock-picks: fungal infection facilitates the intrusion of strangers into ant colonies

Studies investigating host-parasite systems rarely deal with multispecies interactions, and mostly explore impacts on hosts as individuals. Much less is known about the effects at colony level, when parasitism involves host organisms that form societies. We surveyed the effect of an ectoparasitic fungus, Rickia wasmannii, on kin-discrimination abilities of its host ant, Myrmica scabrinodis, identifying potential consequences at social level and subsequent changes in colony infiltration success of other organisms. Analyses of cuticular hydrocarbons (CHCs), known to be involved in insects’ discrimination processes, revealed variations in chemical profiles correlated with the infection status of the ants, that could not be explained by genetic variation tested by microsatellites. In behavioural assays, fungus-infected workers were less aggressive towards both non-nestmates and unrelated queens, enhancing the probability of polygyny. Likewise, parasitic larvae of Maculinea butterflies had a higher chance of adoption by infected colonies. Our study indicates that pathogens can modify host recognition abilities, making the society more prone to accept both conspecific and allospecific organisms.

The effects of fungal infection and physiological condition on the locomotory behaviour of the ant Myrmica scabrinodis

Parasite infection often results in alterations in host behaviour. These changes vary greatly in their magnitude, from slight shifts in the time spent by the host performing a given activity to the appearance of novel behaviours. The effects of parasites can differ with the age and the physiological condition of the host. Rickia wasmannii is an ectoparasitic fungal symbiont in Myrmica ants that covers the whole body surface of the host and reduces its lifespan. The fungus is present in both young and old individuals, making it an optimal subject for the study of age-related parasitic effects. We tested the effect of fungal infection on the locomotory activity of the Myrmica scabrinodis ant in different age categories. The fat content of workers was measured as a proxy for their physiological status. Based on our findings, old workers bore more thalli and were leaner than young individuals, while they tended to move at higher speeds and with a lower degree of meandering. Young individuals covered smaller distances, at slower speeds and with a higher degree of meandering. Contrary to our expectations, the infection intensity of R. wasmannii affected neither the fat content nor the locomotory activity of ant workers. However, the two age classes seem to have different strategies with regards to the relationship between fat content and distance covered. Our results suggest that characteristics of locomotory activity differ between the age classes in many respects, and are also influenced by their physiological status, but parasitism by R. wasmannii does not seem to have a straightforward effect on any of the variables studied.

Antifungal Effect of Silver Nanoparticles on Rickia wasmannii Cavara (Ascomycota: Laboulbeniales) Infecting Myrmica scabrinodis Nylander (Formicidae) Ants

Rickia wasmannii Cavara (Ascomycota: Laboulbeniales) is an ectoparasitic fungus infecting Myrmica ants. Ant-parasitic Laboulbeniales and their interactions with the hosts have been in the focus of several studies. To assess the effects of these fungi, comparison of infected and uninfected or completely treated ants are needed. So far, treating Laboulbeniales infection was only achieved with cockroaches, but not with ants. We present a simple, yet relatively long, AgNP topical treatment that reduces or eliminates Rickia infection from Myrmica scabrinodis ants without affecting their lifespan. We discuss the possibilities of the proposed treatment in the light of the biology of Rickia.

Distribution of the myrmecoparasitic fungus Rickia wasmannii (Ascomycota: Laboulbeniales) across colonies, individuals, and body parts of Myrmica scabrinodis

The ant species Myrmica scabrinodis plays a markedly important ecological role through much of the humid grasslands of Eurasia. It hosts a species-rich community of pathogens and parasites, including Rickia wasmannii, an enigmatic member of entomoparasitic laboulbenialean fungi. This study provides a descriptive ecology of R. wasmannii by characterizing its prevalence and distribution across several hierarchical levels: colonies, individuals, and anatomic body parts. Infections were restricted to a single ant species, M. scabrinodis, and infected colonies occurred predominantly in wet habitats. Infections tended to be highly prevalent within infected colonies, often reaching 100% sample prevalence among workers. Individual infections exhibited an aggregated distribution typical to host-parasite systems. Workers from the aboveground part of nests (presumably older ones acting as foragers) were more infected than those from the belowground part. Fungal thalli could be found all over the body of the hosts, the head and the abdomen being the most infected parts of the body. The fungi’s distribution among host body parts statistically differed between low versus high-intensity infections: the initial dominance of the head decreased with advancing infection. These findings may provide baseline data for future comparative or monitoring studies.

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.

Benomyl treatment decreases fecundity of ant queens

Methyl benzimidazole carbamate fungicides, including benomyl, are widely used in agriculture, and to eliminate entomopathogenic infections. We treated queens of Myrmica rubra (Hymenoptera:Formicidae) infected or not by Rickia wasmannii (Laboulbeniales:Laboulbeniaceae) with benomyl, 1mg/ml p.o. for six weeks. Benomyl did not treat the infection, and the treatment alone caused strong decrease in the fecundity of control healthy queens from 18.0±8.4 to 3.7±5.2eggs per healthy queen. This is the first evidence on severe adverse effects of methyl benzimidazole carbamate fungicide on the fecundity of insects, which might be responsible for altered species composition of ant assemblages in the cultural landscape.

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.

Rickia wasmannii increases the need for water in Myrmica scabrinodis (Ascomycota: Laboulbeniales; Hymenoptera: Formicidae)

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. R.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.

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.

Effects of the ectoparasitic fungus Rickia wasmannii on its ant host Myrmica scabrinodis: changes in host mortality and behavior

Social animals like ants, although seemingly well-armed against parasites because of the protective nature of the social system, are nevertheless exposed to several parasitic organisms, among them fungi of the order Laboulbeniales (Ascomycetes). Rickia wasmannii is one such ectoparasitic fungus that lives on different species of the ant genus Myrmica in Europe. The fungus attaches to the outer layer of the cuticle, while appearing on the surface of the hosts as a setae-like structure. There is little information on the effects of the fungi on the host. Usually it is regarded as neutral, in spite of its high abundance on the ants. We studied the impact of a R.wasmannii infection on the lifespan and grooming behavior of its main host M. scabrinodis in artificial nests in laboratory conditions for 2 months. The lifespan of infected individuals was significantly reduced in comparison with the lifespan of uninfected ants. The frequency of allogrooming was significantly higher in infected nests, while only a marginally significant positive effect could be detected in the case of autogrooming. Increased grooming may either be an effective aspect of host defense or, alternatively, a pathogen-induced behavioral change that enhances pathogen transmission. This study thus provides the first documented evidence of the potential effects of R. wasmannii on its ant hosts.