Open Access
Issue
Parasite
Volume 23, 2016
Article Number 50
Number of page(s) 7
DOI https://doi.org/10.1051/parasite/2016060
Published online 16 November 2016

© W.P. Pfliegler et al., published by EDP Sciences, 2016

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Social symbionts, referred to as “inquilines”, are those insects and other arthropods that live in the nest of their ant hosts (Hymenoptera: Formicidae) and have some obligatory, symbiotic relationship with them. These symbionts can be parasites, commensals, or mutualists. Relationships between ants and their diverse inquiline (= myrmecophilous) arthropod species (mites, isopods, springtails, bristletails, crickets, flies, butterflies, beetles, etc. [18]) are shaped by multiple factors. Inquilines are greeted with a stable microclimate, abundant food, protection from predators, and protection from most microbial pathogens by a “social immunity” in the ant nest “microhabitat” [14, 18, 21, 24, 34, 36, 37]. This social immunity generally results in reduced virulence. As a result, parasites of insect societies are thought to be less damaging to their hosts than those associated with non-social hosts [19]. Ant colonies, on the other hand, can harbor a diversity of highly specialized parasitic microorganisms [18, 45] and the possibility of myrmecophilous arthropods acquiring some of these associates cannot be excluded.

Laboulbeniales biotrophic parasites

The Laboulbeniales (Fungi: Ascomycota: Laboulbeniomycetes) represent a highly diversified but understudied example of fungal biotrophs that live attached to the exterior of their arthropod hosts. Hosts are members of three subphyla in the Arthropoda: Chelicerata, Myriapoda, and Hexapoda. Six species of this order are associated with ants: Dimorphomyces formicicola (Speg.) I.I. Tav., Laboulbenia camponoti S.W.T. Batra, L. ecitonis G. Blum, L. formicarum Thaxt., Rickia lenoirii Santam., and R. wasmannii Cavara [12, 13, 16, 17, 34].

Host shifts are probably an important driving force of speciation among Laboulbeniales fungi [11], as certain morphologically similar species are associated with phylogenetically unrelated hosts. For example, Laboulbenia davidsonii W. Rossi was described from cicindeline hosts (Coleoptera: Carabidae: Cicindelinae), although it is obviously related to a group of species parasitic on Galerita spp. (Coleoptera: Carabidae: Harpalinae) [30]. In addition, L. littoralis De Kesel & Haelew. and L. slackensis Cépède & F. Picard are sister taxa that also occur on two unrelated beetle hosts, Cafius xantholoma (Gravenhorst, 1806) (Coleoptera: Staphylinidae: Staphylininae) and Pogonus chalceus (Marsham, 1802) (Coleoptera: Carabidae: Trechinae), respectively. These hosts, however, are both halobiont, salt marsh-inhabiting species and occur in close proximity to seaweed and plant debris. Morphological and ecological evidence supported that a host shift between these unrelated but co-occurring hosts had happened, leading to reproductive isolation of populations (on these different hosts), changes in morphology, and speciation [11].

Plurivory of Laboulbeniales is an interesting phenomenon. First, most Laboulbeniales exhibit moderate to high host specificity. Often there is a one-to-one relationship between parasite and host. Thus, explaining how and why certain Laboulbeniales species have multiple hosts is difficult. Second, plurivory could ultimately lead to (ecological) speciation by reproductive isolation, since the different populations may be using different nutritional resources and environments. It has been suggested that specific nutrients of co-habiting hosts (or, alternatively, nutrients available from the hosts’ environment) may be far more important for Laboulbeniales species associated with multiple hosts than the identity of the insect hosts [3, 11, 37]. The best-known example of a Laboulbeniales species with multiple diverse host groups is L. ecitonis, reported in Brazil [7], Costa Rica [27], Ecuador [29], and Panama (Haelewaters, unpublished data). This fungus is known from Eciton Latreille, 1804 ants (Ecitoninae), Sternocoelopsis auricomus Reichensperger, 1923 (Coleoptera: Histeridae), Ecitophya spp. (Coleoptera: Staphylinidae), and uropodid mites (Acari: Mesostigmata: Uropodidae). These beetle and mite species are all associated with the Eciton ants.

The genus Rickia

Two of the six Laboulbeniales species associated with ants belong to the genus Rickia Cavara. The most widespread species of the two is R. wasmannii, with reports from 17 European countries; it is found on 9 species in the genus Myrmica Latreille, 1804 [12, 16]. The second species, R. lenoirii, is known from Messor wasmanni Krausse, 1910 and M. structor (Latreille, 1798) in France, Greece, Hungary, and Romania [2, 34].

The genus Rickia includes many more species (a total of 161) [35] and is unusual among Laboulbeniales for several reasons. Morphologically, its receptacle is multiseriate (mostly triseriate) and one cell layer thick. Its host distribution is very wide, encompassing three subphyla: Chelicerata (mites), Myriapoda [millipedes (Diplopoda)], and Hexapoda [ants (Hymenoptera: Formicidae), cockroaches (Blattodea), mole crickets (Orthoptera), and various beetle families (Coleoptera)] [39, 44]. Rickia species also differ largely in size. The largest species was only recently described: R. gigas Santam et al., measuring up to 2.2 mm in total length. This is among the largest species in the order Laboulbeniales [32, 35]. Among the smallest Rickia species, most of them are “acarophilous”, that is, they occur on mites. Examples are R. anomala (48–56 μm), R. depauperata (35–40 μm), R. excavata (75–85 μm), and R. parvula (40 μm) [42]. However, other small Rickia species have also been described that are not associated with mites, such as R. euxesti (40–68 μm) on Euxestus spp. (Coleoptera, Cerylonidae), and R. lenoirii (45–67 μm) on Messor spp. (Hymenoptera, Formicidae) [34, 42].

In this study, we screened Myrmica scabrinodis Nylander, 1846 ants and associated myrmecophilous arthropods for possible infections with a well-known and easily recognized Laboulbeniales ectoparasite, Rickia wasmannii [8], in populations from Hungary. This fungus is only known to infect nine species of the genus Myrmica [17] and it is remarkable for its well-studied biology and effects on its hosts [1, 9, 16, 17, 23]. Myrmica ants are known to host several parasitic and inquiline arthropods in Central Europe: mites, larvae of Microdon myrmicae Schönrogge et al. 2002 (Diptera: Syrphidae) and Maculinea van Eecke, 1915 caterpillars (Lepidoptera: Lycaenidae) [45], all of which can co-occur within the same sites [40].

Materials and methods

Ant colonies of Myrmica scabrinodis were collected in 2015 at the following sites in eastern and northern Hungary (Figure 1): 2 colonies from Gyöngyös: Sár-hegy: Gyilkos-rét (47°48′ N, 19°58′ E; 352 m a.s.l.); 3 colonies from Újléta (47°26′ N, 21°51′ E; 120 m a.s.l.); and 2 colonies from Rakaca: Meszes (48°27′ N, 20°47′ E; 165 m a.s.l.). We screened 60 workers for infection with R. wasmannii from each colony. Additionally, 1 syrphid larva (Diptera: Syrphidae) from Rakaca: Meszes (collected in 2012) and smaller collections of worker ants from Rakaca: Meszes (2014) and from Jósvafő: Tohonya-hát (48°29′ N, 20°32′ E; 268 m a.s.l) (2015) were screened for infection.

thumbnail Figure 1.

Collection sites in Hungary. A: Gyöngyös: Sár-hegy: Gyilkos-rét. B: Újléta. C: Rakaca: Meszes. D: Jósvafő: Tohonya-hát.

Ants and their associates were killed in ethanol and screened for fungal infection using a Leica MZ125 microscope at 10–160× magnification. Mites were mounted onto microscope slides in Heinz PVA Mounting Medium and screened at 10–100× magnification using a Carl Zeiss microscope with transmitted light.

Host species were determined according to [25] (ants) and [20] (mites). Fungal thalli were determined following [8, 12]. Immature thalli were determined based on the characteristically on the characteristically elongated basal cell of the thallus (= cell I).

Results

Table 1 summarizes numbers of screened and infected ants and inquilines per M. scabrinodis colony. A total of 426 M. scabrinodis workers were collected and screened for Laboulbeniales. Four hundred twenty workers were infected with R. wasmannii (= 98.6%). In the sampled colonies, 62 mite specimens were found belonging to four families: Acaridae (n = 40), Histiostomatidae (n = 18), Neopygmephoridae (n = 1), and Scutacaridae (n = 1). The vast majority were phoretic deutonymphs of the Astigmatina “cohort”, which include the Acaridae and Histiostomatidae families. Altogether, 6 infected deutonymphs in the Acaridae family from a single colony in Gyöngyös: Gyilkos-rét were found (= 9.7% of all screened mites). In this colony, 33% of the Acaridae deutonymphs were infected, but none of the Histiostomatidae deutonymphs. All infected specimens bore 1 to 3 immature thalli. An example of an infected mite is shown in Figure 2a, with a mature thallus isolated from a M. scabrinodis worker for comparison (Fig. 2b). This is the first non-ant host record for R. wasmannii.

thumbnail Figure 2.

Rickia wasmannii. (a): Infected Acaridae deutonymph with three immature R. wasmannii thalli attached (marked). (b): Mature thallus from a Myrmica scabrinodis ant host. Scale bar = 200 μm.

Table 1.

Ants and ant colonies collected in Hungary, in the period 2012–2015, with indication of number of screened and infected ants and inquilines.

Furthermore, two immature Rickia thalli are reported on the anterior horn of a Microdon myrmicae larva from a colony collected in Rakaca. This represents the first report of any Rickia species on Diptera.

Discussion

The nature of the relationships between R. wasmannii and its newly recorded hosts pose several questions and imply parallels with other host-parasite relations within the Laboulbeniales order. Species of Laboulbeniales associated with mites are frequently found on the mites’ various host beetles as well [38, 42]. However, in many cases the parasite has only been recorded from the mite but not on its host insect [33, 38, 42]. Phoretic states of Pyxidiophora Bref. & Tavel (Pyxidiophorales, sister order of Laboulbeniales) are also relatively frequently reported on beetle-associated phoretic mites [46].

Of all Rickia species, 59 have been described from mites [22, 34, 41, 42]. Many of these are found exclusively on insect-associated mites (mostly those associated with Coleoptera) but not on the insects [33, 41, 42]. For example, three species of Rickia from Poland were described [22] on myrmecophilous mites belonging to different families of the order Mesostigmata from nests of Lasius spp. Neither of these Rickia species was found on the ants. Upon the discovery of R. lenoirii from Messor ants, its similarity to these extremely small mite-associated species was noted, suggesting that R. lenoirii may have evolved after a host shift from mites to ants [34]. Also in the case of R. euxesti, a species occurring on Cerylonidae, host shifts from associated mites to the beetle host could have happened [sensu 38, 41]. Another Rickia species, R. kistneri, was found on >50% of the Mimaenictus wilsoni Kistner & Jacobson, 1975 specimens (Coleoptera: Staphylinidae) [29]. These myrmecophilous beetles were collected together with >100 Aenictus laeviceps ants in the same emigrating column. However, none of the ants were infected [29]. Some species of the genus Rickia reported from ant species and/or their inquilines are listed in Table 2.

Table 2.

Rickia parasitizing ants and/or associated (myrmecophilous) arthropods, with indication of the currently known distribution.

Ecological dead-ends?

Our report of Rickia thalli on a single Microdon myrmicae larva represents the first report of any species of Laboulbeniales on Syrphidae. The extremely low parasite load on the relatively large M. myrmicae larva (two immature thalli) indicates that this infection may have been accidental. Laboulbeniales occur practically exclusively on adults. Infections of eggs, larvae, pupae, or nymphs are extremely rare, but have been reported in cockroaches, termites, beetles, and ants [3, 28, 31]. In cockroaches, Herpomyces spp. are found on both the adults and co-habiting nymphs, although upon ecdysis, the infection is lost [28]. As to beetles, a single immature specimen of Systena s-littera (Linnaeus, 1758) from Brazil was reported to carry Laboulbenia systenae Speg. [31].

The infected mites and the single M. myrmicae larva bore only immature thalli. We cannot exclude the possibility that using alternative hosts may be deleterious for the fungus. Alternative hosts thus may provide only suboptimal conditions for the fungus. Furthermore, mite deutonymphs and fly larvae both undergo ecdysis and thus Laboulbeniales thalli will be lost [sensu 28]. In these cases, the accidental colonization of new hosts may be dead-ends for R. wasmannii. Further studies on the highly diverse arthropod community of Myrmica nests [45] could identify more hosts of R. wasmannii and help in answering questions about the life history strategies of this parasite.

Microhabitats

Rickia wasmannii making use of multiple hosts in a different order (Diptera) and even a different subphylum (Chelicerata) as described here reminisces the tropical L. ecitonis on inquilines of Eciton ants [3, 7]. In this case, the ant colony itself (of which the individual members form a “living nest”) serves as a “microhabitat” where ascospores can be transmitted to unusual myrmecophilous hosts. Other examples of a microhabitat are saltmarshes, subterranean caves, and wet, decomposing logs [11, 26, 38]. Several complex associations between log-inhabiting arthropods, their associated mites, and Rickia (as well as Dimorphomyces) species were described from Queensland, Australia [38]. Rickia berlesiana was found to be the most plurivorous one, recorded from several species of Fedrizziidae (Acari: Mesostigmata) as well as three species of Passalidae beetles hosting the mites [38]. These results indicate the use of multiple alternative hosts in two subphyla.

The presence of R. wasmannii on inquilines in Myrmica ant nests suggests that R. wasmanni may have adapted to the ant nest environment and is less dependent on acquiring specific nutrients from the hosts. In other words, ecological specificity is more important than host specificity. Tragust et al. [43] have shown that R. wasmannii has a non-penetrating hoof-like foot structure for attachment to the host. The fact that this species does not penetrate its host calls for another mode for nutrition. If R. wasmannii only needs the host for attachment to the cuticle, it could indeed be that nutrition happens at the cuticle or through the environment. This may explain why R. wasmannii does not need to be host specific because of restricted nutritional needs.

Ecological specificity

The “easiness” of using non-ant hosts is particularly compelling when the apparent narrow host specificity of R. wasmannii is taken into account. Haelewaters et al. [16], for example, found no sign of transmission between infected Myrmica spp. and ants of other genera sharing the same narrow geographic area. The key factor enabling the usage of non-ant hosts may be the microhabitat, provided by the nest of the Myrmica ants: apparently, the fungus exhibits low host specificity, but only inside the ant nest microhabitat. Our records thus represent the third type of specificity alongside the well-known host specificity [10] and position specificity [15] in the order Laboulbeniales: ecological specificity [11].

Based on our observations, we do not know with certainty whether infection on inquilines in nests of M. scabrinodis is truly due to the fact that they represent alternative hosts (or even stable hosts shift events) for the fungus, or whether infection on inquilines represents chance events. However, the occurrence of infection on associated myrmecophiles may, over evolutionary time, lead to the use of myrmecophiles as alternative hosts for the fungus and, because of micro-evolutionary changes and reproductive isolation, potentially even to speciation.

Acknowledgments

WPP was supported through the New National Excellence Program of the Ministry of Human Capacities of Hungary. AT was supported by the “AntLab” Marie Curie Career Integration Grant, part the 7th European Community Framework Programme, and by a “Bolyai János” scholarship of the Hungarian Academy of Sciences (MTA). DH was supported by the David Rockefeller Center for Latin American Studies at Harvard University. Figure 1 was produced using a map from http://www.d-maps.com/. We thank an anonymous reviewer as well as the Editor-in-Chief Dr. Jean-Lou Justine for comments and suggestions.

References

  1. Báthori F, Csata E, Tartally A. 2015. Rickia wasmannii increases the need for water in Myrmica scabrinodis (Ascomycota: Laboulbeniales; Hymenoptera: Formicidae). Journal of Invertebrate Pathology, 126, 78–82. [CrossRef] [PubMed] [Google Scholar]
  2. Báthori F, Pfliegler WP, Tartally A. 2015. First records of the recently described ectoparasitic Rickia lenoirii Santam. (Ascomycota: Laboulbeniales) in the Carpathian Basin. Sociobiology, 62, 620–622. [CrossRef] [Google Scholar]
  3. Benjamin R. 1971. Introduction and supplement to Roland Thaxter’s contribution towards a monograph of the Laboulbeniaceae. Bibliotheca Mycologica, 30, 1–155. [Google Scholar]
  4. Blackwell M. 1986. A new species of Phyxidiophora and its Thaxteriola anamorph. Mycologia, 78, 605–612. [CrossRef] [Google Scholar]
  5. Blackwell M. 1994. Minute mycological mysteries: the influence of arthropods on the lives of fungi. Mycologia, 86, 1–17. [CrossRef] [Google Scholar]
  6. Blackwell M, Bridges JR, Moser JC, Perry TJ. 1986. Hyperphoretic dispersal of a Pyxidiophora anamorph. Science, 232, 993–995. [CrossRef] [PubMed] [Google Scholar]
  7. Blum G. 1924. Zwei neue Laboulbenien aus Brasilien. Centralblatt für Bakteriologie, - Parasitenkunde und Infektionskrankheiten, Zweite Abteilung, 62, 300–302. [Google Scholar]
  8. Cavara F. 1899. Di una nuova Laboulbeniacea: Rickia wasmannii, nov. gen. et nov. spec. Malpighia, 13, 173–188. [Google Scholar]
  9. Csata E, Erős K, Markó B. 2014. Effects of the ectoparasitic fungus Rickia wasmannii on its ant host Myrmica scabrinodis: changes in host mortality and behavior. Insectes Sociaux, 61, 247–252. [CrossRef] [Google Scholar]
  10. De Kesel A. 1996. Host specificity and habitat preference of Laboulbenia slackensis. Mycologia, 88, 565–573. [CrossRef] [Google Scholar]
  11. De Kesel A, Haelewaters D. 2014. Laboulbenia slackensis and L. littoralis sp. nov. (Ascomycota, Laboulbeniales), two sibling species as a result of ecological speciation. Mycologia, 106, 407–414. [CrossRef] [PubMed] [Google Scholar]
  12. De Kesel A, Haelewaters D, Dekoninck W. 2016. Myrmecophilous Laboulbeniales (Ascomycota) in Belgium. Sterbeeckia, 34, 3–6. [Google Scholar]
  13. Espadaler X, Santamaria S. 2012. Ecto- and endoparasitic fungi on ants from the Holarctic Region. Psyche, 2012, 1–12. [CrossRef] [Google Scholar]
  14. Geiselhardt SF, Peschke K, Nagel P. 2007. A review of myrmecophily in ant nest beetles (Coleoptera: Carabidae: Paussinae): linking early observations with recent findings. Naturwissenschaften, 94, 871–894. [CrossRef] [PubMed] [Google Scholar]
  15. Goldmann L, Weir A. 2012. Position specificity in Chitonomyces (Ascomycota, Laboulbeniomycetes) on Laccophilus (Coleoptera, Dytiscidae): a molecular approach resolves a century-old debate. Mycologia, 104, 1143–1158. [CrossRef] [PubMed] [Google Scholar]
  16. Haelewaters D, Boer P, Noordijk J. 2015. Studies of Laboulbeniales (Fungi, Ascomycota) on Myrmica ants: Rickia wasmannii in the Netherlands. Journal of Hymenoptora Research, 44, 39–47. [Google Scholar]
  17. Haelewaters D, Gort G, Boer P, Noordijk J. 2015. Studies of Laboulbeniales (Fungi, Ascomycota) on Myrmica ants (II): variation of infection by Rickia wasmannii over habitats and time. Animal Biology, 65, 219–231. [CrossRef] [Google Scholar]
  18. Hölldobler B, Wilson EO. 1990. The ants. Springer-Verlag: Berlin, Germany. [Google Scholar]
  19. Hughes DP, Pierce NE, Boomsma JJ. 2008. Social insect symbionts: evolution in homeostatic fortresses. Trends in Ecology and Evolution, 23, 672–677. [CrossRef] [Google Scholar]
  20. Krantz GW, Gerald W, Walter DE. 2009. A manual of acarology. Texas Tech University Press: Lubbock, Texas. [Google Scholar]
  21. Kronauer DJC, Pierce NE. 2011. Myrmecophiles. Current Biology, 21, R208–R209. [CrossRef] [Google Scholar]
  22. Majewski T. 1994. The Laboulbeniales of Poland. Polish Botanical Studies, 7, 1–466. [Google Scholar]
  23. Markó B, Csata E, Erős K, Német E, Czekes Z, Rózsa L. 2016. Distribution of the myrmecoparasitic fungus Rickia wasmannii (Ascomycota: Laboulbeniales) across colonies, individuals, and body parts of Myrmica scabrinodis. Journal of Invertebrate Pathology, 136, 74–80. [CrossRef] [PubMed] [Google Scholar]
  24. Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA. 2002. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annual Review of Entomology, 47, 733–771. [CrossRef] [PubMed] [Google Scholar]
  25. Radchenko A, Elmes GW. 2010. Myrmica ants (Hymenoptera: Formicidae) of the Old World. Natura Optima Dux Foundation: Warsaw, Poland. [Google Scholar]
  26. Reboleira ASPS, Fresneda J, Salgado JM. 2016. A new species of Speonemadus from Portugal with the revision of the escalerai-group (Coleoptera: Leiodidae). European Journal of Taxonomy, in press. [Google Scholar]
  27. Reichensperger A. 1935. Beitrag zur Kenntnis der Myrmekophilen-fauna Brasiliens under Costa Ricas III. (Col. Staphyl. Hist.). Arbeiten über morphologische und taxonomische Entomologie aus Berlin-Dahlem, 2, 188–218 + Tafel 3. [Google Scholar]
  28. Richards AG, Smith MN. 1955. Infection of cockroaches with Herpomyces (Laboulbeniales). I. Life history studies. Biological Bulletin, 108, 206–218. [CrossRef] [Google Scholar]
  29. Rossi W. 1991. A new species and a new record of Laboulbeniales Ascomycetes parasitic on myrmecophilous Staphylinidae. Sociobiology, 182, 197–202. [Google Scholar]
  30. Rossi W. 2011. New species of Laboulbenia from Ecuador, with evidence for host switch in the Laboulbeniales. Mycologia, 103, 184–194. [CrossRef] [PubMed] [Google Scholar]
  31. Rossi W, Bergonzo E. 2008. New and interesting Laboulbeniales from Brazil. Aliso, 26, 1–8. [CrossRef] [Google Scholar]
  32. Rossi W, Haelewaters D, Pfister DH. 2016. Fireworks under the microscope: a spectacular new species of Zodiomyces from the Thaxter collection. Mycologia, 108, 709–715. [CrossRef] [PubMed] [Google Scholar]
  33. Samšináková A. 1968. Nález houby Dimeromyces falcatus Paoli (Laboulbeniales) na novém hostiteli [Fund des Pilzes Dimeromyces falcatus Paoli (Laboulbeniales) auf einem neuen Wirt]. Czech Mycology, 22, 225–228. [Google Scholar]
  34. Santamaria S, Espadaler X. 2015. Rickia lenoirii, a new ectoparasitic species, with comments on world Laboulbeniales associated with ants. Mycoscience, 56, 224–229. [CrossRef] [Google Scholar]
  35. Santamaría S, Enghoff H, Reboleira ASPS. 2016. Hidden biodiversity revealed by collections-based research – Laboulbeniales in millipedes: genus Rickia. Phytotaxa, 243, 101–127. [CrossRef] [Google Scholar]
  36. Schär S, Larsen LLM, Meyling NV, Nash DR. 2015. Reduced entomopathogen abundance in Myrmica ant nests-testing a possible immunological benefit of myrmecophily using Galleria mellonella as a model. Royal Society Open Science, 2, 150474. [CrossRef] [PubMed] [Google Scholar]
  37. Scheloske H. 1969. Beiträge zur Biologie, Ökologie und Systematik der Laboulbeniales (Ascomycetes) unter besondere Berücksichtigung des Parasit-Wirt-Verhältnisses. Parasitologische Schriftenreihe, 19, 1–176. [Google Scholar]
  38. Seeman OD, Nahrung HF. 2000. Mites as fungal vectors? The ectoparasitic fungi of mites and their arthropod associates in Queensland. Australasian Mycologist, 19, 3–9. [Google Scholar]
  39. Sugiyama K. 1978. The Laboulbeniomycetes of eastern Asia. 2. On eight species from Japan and Formosa including two new species of Rickia. Journal of Japanese Botany, 53, 154–160. [Google Scholar]
  40. Tartally A. 2008. Myrmecophily of Maculinea butterflies in the Carpathian Basin (Lepidoptera: Lycaenidae). University of Debrecen: Debrecen, Hungary. [Google Scholar]
  41. Tavares II. 1985. Laboulbeniales (Fungi, Ascomycetes). Mycological Memoirs, 9, 1–627. [Google Scholar]
  42. Thaxter R. 1926. Contribution towards a monograph of the Laboulbeniaceae. Part IV. Memoirs of the American Academy of Arts and Sciences, 15, 431–555. [CrossRef] [Google Scholar]
  43. Tragust S, Tartally A, Espadaler X, Billen J. 2016. Histopathology of Laboulbeniales (Ascomycota: Laboulbeniales): ectoparasitic fungi on ants (Hymenoptera: Formicidae). Myrmecological News, 23, 81–89. [Google Scholar]
  44. Weir A. 1998. Notes on the Laboulbeniales of Sulawesi. The genus Rickia. Mycologia, 102, 327–343. [Google Scholar]
  45. Witek M, Barbero F, Markó B. 2014. Myrmica ants host highly diverse parasitic communities: from social parasites to microbes. Insectes Sociaux, 61, 307–323. [CrossRef] [Google Scholar]

Cite this article as: Pfliegler WP, Báthori F, Haelewaters D & Tartally A: Studies of Laboulbeniales on Myrmica ants (III): myrmecophilous arthropods as alternative hosts of Rickia wasmannii. Parasite, 2016, 23, 50.

All Tables

Table 1.

Ants and ant colonies collected in Hungary, in the period 2012–2015, with indication of number of screened and infected ants and inquilines.

Table 2.

Rickia parasitizing ants and/or associated (myrmecophilous) arthropods, with indication of the currently known distribution.

All Figures

thumbnail Figure 1.

Collection sites in Hungary. A: Gyöngyös: Sár-hegy: Gyilkos-rét. B: Újléta. C: Rakaca: Meszes. D: Jósvafő: Tohonya-hát.

In the text
thumbnail Figure 2.

Rickia wasmannii. (a): Infected Acaridae deutonymph with three immature R. wasmannii thalli attached (marked). (b): Mature thallus from a Myrmica scabrinodis ant host. Scale bar = 200 μm.

In the text

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.