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Infectious intimacy and contaminated caves—three new species of ectoparasitic fungi (Ascomycota: Laboulbeniales) from blaniulid millipedes (Diplopoda: Julida) and inferences about their transmittal mechanisms

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Abstract

Laboulbeniales is an order of more than 2000 species of small ascomycete fungi which are ectoparasites of insects, millipedes and mites. They are often highly host-specific and often are also highly specific with regard to which body parts they infect. Laboulbeniales from millipedes are particularly poorly known—only 12 species have been described until now, mostly from Europe. Here, we describe the first laboulbeniaceous parasites from blaniulid millipedes: Troglomyces bilabiatus from Acipes spp., Troglomyces pusillus from Iberoiulus cavernicola Ceuca, 1967 and Troglomyces triandrus from Archiboreoiulus palidus (Brade-Birks, 1920). The generic description of Troglomyces is emended. Different types of site specificity of the three new parasites, as well as of previously described species, are explained in terms of aspects of host biology: mating behaviour and habitat. Species from epigean hosts tend to show a high degree of site specificity suggesting transfer during host copulation, whereas most species from cave hosts show no pronounced site specificity and are probably transferred via the substrate. Possible roles of host defensive secretions and parthenogenesis in relation to infection with Laboulbeniales are briefly discussed.

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References

  • Andersen, J., & Skorping, A. (1991). Parasites of carabid beetles: prevalence depends on habitat selection of the host. Canadian Journal of Zoology, 69, 1216–1220.

    Article  Google Scholar 

  • Arwidsson, T. (1946). Om svenska laboulbeniacefynd. Svensk Botanisk Tidskrift, 40, 307–309.

    Google Scholar 

  • Bechet, M. & Bechet, I. (1986). Rickia pachyiuli n. sp. (Ascomycetes, Laboulbeniales) parazita pe Pachyiulus hungaricus (Karsch.) (Diplopoda, Iulidae). Contributii Botanice, Cluj-Napoca, 1986, 31-34.

  • Benjamin, R. K. (1971). Introduction and supplement to Roland Thaxter's contribution towards a monograph of the Laboulbeniaceae. Bibliotheca Mycologica, 30, 1–155.

    Google Scholar 

  • Benjamin, R. K., & Shanor, L. (1952). Sex of host specificity and position specificity of certain species of Laboulbenia on Bembidion picipes. American Journal of Bottany, 39, 125–131.

    Article  Google Scholar 

  • Biernaux, J., & Baurant, R. (1964). Observations sur l’hibernation de Archiboreoiulus pallidus Br.-Bk. (Myriapoda-Diplopode-Iulidae). Bulletin de l’Institut agronomique et des Stations de Recherches de Gembloux, 32, 290–298.

    Google Scholar 

  • Blackwell, M., & Malloch, D. (1989). Similarity of Amphoromorpha and secondary capilliconidia of Basidiobolus. Mycologia, 81, 735–741.

    Article  Google Scholar 

  • Blower, J. G. (1974). Food consumption and growth in a laboratory population of Ophyiulus pilosus (Newport). Symposia of the zoological Society of London, 32, 527–551.

    Google Scholar 

  • Bodner, M., & Raspotnig, G. (2012). Millipedes that smell like bugs: (E)-alkenals in the defensive secretion of the julid diplopod Allajulus dicentrus. Journal of Chemical Ecology, 38, 547–556. doi:10.1007/s10886-012-0127-5.

    Article  CAS  PubMed  Google Scholar 

  • Breny, R., & Biernaux, J. (1966). Diplopodes Belges: Position systématique et biotopes. Bulletin and Annales de la Société Royale d’Entomologie de Belgique, 102, 269–326.

    Google Scholar 

  • Brookes, C. H., & Willoughby, J. (1978). An investigation of the ecology and life history of the millipede Blaniulus guttulatus (Bosc) in a British woodland. Abhandlungen und Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg (NF), 21(22), 105–144.

    Google Scholar 

  • Colla, S. (1932). “Troglomyces Manfredii” n. gen. et n. sp.: nuova Laboulbeniacea sopra un miriapode. Nuovo Giornale Botanico Italiano, 39, 450–453.

    Article  Google Scholar 

  • De Kesel, A. (1993). Relations between host population density and spore transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales) from Pogonus chalceus (Coleoptera, Carabidae). Belgian Journal of Botany, 126(2), 155–163.

    Google Scholar 

  • De Kesel, A. (1995). Relative importance of direct and indirect infection in the transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales). Belgian Journal of Botany, 128(2), 124–130.

    Google Scholar 

  • De Kesel, A., Haelewaters, D., & Gerstmans, C. (2013). Two interesting species of Rickia (Laboulbeniales) from coastal habitats in Belgium and the Netherlands. Sterbeeckia, 32, 6–10.

    Google Scholar 

  • 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(3), 407–414. doi:10.3852/13-348.

    Article  PubMed  Google Scholar 

  • Eisner, T., Alsop, D., Hicks, K., & Meinwald, J. (1978). Defensive secretions of millipedes. In S. Bettini (Ed.), Arthropod Venoms, Handbook of Experimental Pharmacology (Vol. 48, pp. 41–72). Berlin: Springer.

    Chapter  Google Scholar 

  • Enghoff, H. (1983). Acipes—a Macaronesian genus of millipedes (Diplopoda, Julida, Blaniulidae). Steenstrupia, 9, 137–179.

    Google Scholar 

  • Enghoff, H., & Reboleira, A. S. P. S. (2013). Subterranean species of Acipes Attems, 1937 (Diplopoda, Julida, Blaniulidae). Zootaxa, 3652, 485–491. doi:10.11646/zootaxa.3652.4.6.

    Article  Google Scholar 

  • Enghoff, H., & Reboleira, A. S. P. S. (2014). Redescription of Iberoiulus cavernicola Ceuca, 1967, and the relationships of the genus Iberoiulus Mauriès, 1985 (Diplopoda, Julida, Blaniulidae). Zootaxa, 3869, 153–158. doi:10.11646/zootaxa.3869.2.4.

    Article  PubMed  Google Scholar 

  • Kevan, D. K. M. E. (1983). A preliminary survey of known and potentially Canadian millipedes (Diplopoda). Canadian Journal of Zoology, 61, 2956–2975.

    Article  Google Scholar 

  • Kime, R. D. (2004). The Belgian millipede fauna (Diplopoda). Bulletin d l’Institut Royal des Sciences naturelles en Belgique, Entomologie, 74, 35–68.

    Google Scholar 

  • Kime, R.D. and Enghoff, H. (in prep.) Atlas of European millipedes 2. Julida.

  • Kuwahara, Y., Ômura, H., & Tanabe, T. (2002). 2-Nitroethenylbenzenes as natural products in millipede defense secretions. Naturwissenschaften, 89, 308–310. doi:10.1007/s00114-002-0328-9.

    Article  CAS  PubMed  Google Scholar 

  • Lehtonen, J., Jennions, M. D., & Kokko, H. (2012). The many costs of sex. Trends in Ecology and Evolution, 27, 172–178.

    Article  PubMed  Google Scholar 

  • Lindroth, C. H. (1948). Notes on the ecology of Laboulbeniaceae infesting carabid beetles. Svensk Botanisk Tidskrift, 42, 34–41.

    Google Scholar 

  • Lohmander, H. (1925). Sveriges diplopoder. Kungliga Vetenskaps- och Vitterhets-Samhälles Handlingar, Fjärde Följden, 30(2), 1–115.

    Google Scholar 

  • Majewski, T. (1974). Rare and new Laboulbeniales from Poland. V. Acta Mycologica, 10(2), 267–282.

    Article  Google Scholar 

  • Makarov, S. E., Dimkić, I.Z., Antić, D. Ž., Vujisić, L. V., Stević, T.R., Mitić, B. M., Tomićm V. T., Ilić, B. S., Ćurčić, B. P.M. & Stanković, S.M. (2014). Pachyiulus hungaricus (Karsch, 1881) (Myriapoda, Diplopoda, Julidae)—a model-system for semiochemical analysis and antimicrobial testing. In Tuf, I.H. & Tajovský, K. (eds.) 16th International Congress of Myriapodology. Book of Abstracts (p. 51). Olomouc: Institute of Soil Biology, BC ASCR & Faculty of Science, Palacký University.

  • Mauriès, J.-P. (1969). Observations sur la biologie (sexualité, périodomorphose) de Typhloblaniulus lorifer consoranensis Brölemann (Diplopoda, Blaniulidae). Annales de Spéléologie, 24, 495–504.

    Google Scholar 

  • Minelli, A., & Fusco, G. (2013). Arthropod postembryonic development. In A. Minelli, G. Boxshall, & G. Fusco (Eds.), Arthropod Biology and Evolution. Molecules, Development, Morphology (pp. 91-122). Berlin: Springer.

    Google Scholar 

  • Palmén, E. (1949). The Diplopoda of eastern Fennoscandia. Annales Zoologici Societatis Zoologicæ Botanicæ Fennicæ ‘Vanamo’, 13(6), i-iv + 1-53

  • Pierrard, G., & Biernaux, J. (1974). Note à propos des Diplopodes nuisible aux cultures tempérés et tropicales. Symposia of the zoological Society of London, 32, 629–643.

    CAS  Google Scholar 

  • Prisnyi, A. V. (2001). A review of the millipede fauna of the south of the Middle-Russian Upland, Russia (Diplopoda). Arthropoda Selecta, 10, 297–305.

    Google Scholar 

  • Roncadori, R. W., Duffey, S. S., & Blum, M. S. (1985). Antifungal activity of defensive secretions of certain millipedes. Mycologia, 77(2), 185–191.

    Article  Google Scholar 

  • Rossi, W., & Balazuc, J. (1977). Laboulbéniales parasites de myriapodes. Revue de Mycologie, 41, 525–535.

    Google Scholar 

  • Rossi, W., & Kotrba, M. (2004). A new polymorphic species of Laboulbenia parasitic on a South American fly. Mycological Research, 108, 1315–1319.

    Article  PubMed  Google Scholar 

  • Rossi, W., & Proaño Castro, A. C. (2009). New species of Rhachomyces from Ecuador, one of which is dimorphic. Mycologia, 101, 674–680.

    Article  PubMed  Google Scholar 

  • Rossi, W., & Santamaria, S. (2014). New species of Aporomyces. Turkish Journal of Botany. doi:10.3906/bot-1404-104.

    Google Scholar 

  • Rossi, W., & Weir, A. (1998). Triainomyces, a new genus of Laboulbeniales on the pill-millipede Procyliosoma tuberculatum from New Zealand. Mycologia, 90, 282–289.

    Article  Google Scholar 

  • Santamaria, S., & Faille, A. (2009). New species of Laboulbenia and Rhachomyces (Laboulbeniales, Ascomycota), some of them polymorphic, parasitic on termiticolous ground beetles from tropical Africa. Nova Hedwigia, 89, 97–120.

    Article  Google Scholar 

  • Santamaria, S., Enghoff, H., & Reboleira, A.S.P.S. (2014). Laboulbeniales on millipedes: Diplopodomyces and Troglomyces. Mycologia, XXX.

  • Scheloske, H. W. (1969). Beiträge zur Biologie, Ökologie und Systematik der Laboulbeniales (Ascomycetes) unter besonderer Berücksichtigung des Parasit-Wirt-Verhältnisses. Parasitologische Schriftenreihe, 19, 1–176.

    Google Scholar 

  • Scheloske, H. W. (1976a). Eusynaptomyces benjaminii, spec. nova, (Ascomycetes, Laboulbeniales) und seine Anpassungen an das Fortpflanzungsverhalten seines Wirtes Enochrus testaceus (Coleoptera, Hydrophilidae). Plant Systematics and Evolution, 126, 267–285.

    Article  Google Scholar 

  • Scheloske, H. W. (1976b). Morphologische Anpassungen eines ektoparasitischen Pilzes (Ascomycetes, Laboulbeniales: Misgomyces coneglanensis) an Körperbau und Fortpflanzungsverhalten seines Wirtes (Coleoptera, Hydrophilidae: Laccobius minutus). Entomoliga Germanica, 3, 227–241.

    Google Scholar 

  • Shear, W. A., Jones, T. H., & Miras, H. M. (2007). A possible phylogenetic signal in millipede chemical defenses: the polydesmidan millipede Leonardesmus injucundus Shelley & Shear secretes p-cresol and lacks a cyanogenic defense (Diplopoda, Polydesmida, Nearctodesmidae). Biochemical Systematics and Ecology, 35, 838–842.

    Article  CAS  Google Scholar 

  • Tavares, I. I. (1985). Laboulbeniales (Fungi, Ascomycetes). Mycological Memoirs, 9, 1–627.

    Google Scholar 

  • Thaxter, R. (1908). Contribution towards a monograph of the Laboulbeniaceae. Part II. Memoirs of the American Academy of Arts, 13, 217–469.

    Google Scholar 

  • Vicente, M., & Enghoff, H. (1999). The millipedes of the Canary Islands. Vieraea, 27, 183–204.

    Google Scholar 

  • Voigtländer, K. (1987). Untersuchungen zur Bionomie von Enantiulus nanus (Latzel, 1884) und Allajulus occultus C.L. Koch, 1847 (Diplopoda, Julidae). Abhandlungen und Berichte des Naturkundemuseums Görlitz, 60(10), 1–116.

    Google Scholar 

  • Vujisić, L. V., Makarov, S. E., Ćurčić, B. P. M., Ilić, B. S., Tešević, V. V., Gođevac, D. M., Vučković, I. M., Ćurčić, S. B., & Mitić, B. M. (2011). Composition of the defensive secretion in three species of European millipedes. Journal of Chemical Ecology, 37, 1358–1364.

    Article  PubMed  Google Scholar 

  • Vujisić, L. V., Antić, D. Ž., Vučković, I. M., Sekulić, T. L., Tomić, V. T., Mandić, B. M., Tešević, V. V., Ćurčić, B. P. M., Vajs, V. E., & Makarov, S. E. (2014). Chemical defense in millipedes (Myriapoda, Diplopoda): do representatives of the family Blaniulidae belong to the ‘quinone’ clade? Chemistry and Biodiversity, 11, 483–490.

    Article  PubMed  Google Scholar 

  • Weatherston, J., Tyrrell, D., & Percy, J. E. (1971). Long chain alcohol acetates in the defensive secretion of the millipede Blaniulus guttulatus. Chemistry and Physics of Lipids, 7, 98–100.

    Article  CAS  Google Scholar 

  • Weir, A., & Beakes, G. (1996). Correlative light- and scanning electon miron microscope studies on the developmental morphology of Hesperomyces virescens. Mycologia, 88(5), 677–693.

    Article  Google Scholar 

  • Weir, A., & Hughes, M. (2002). The taxonomic status of Corethromyces bicolor from New Zealand, as inferred from morphological, developmental, and molecular studies. Mycologia, 94(3), 483–493.

    Article  PubMed  Google Scholar 

  • Wu, X., Buden, D. W., & Attygalle, A. B. (2007). Hydroquinones from defensive secretion of a giant Pacific millipede, Acladocricus setigerus (Diplopoda: Spirobolidae). Chemoecology, 17, 131–138. doi:10.1007/s00049-007-0372-1.

    Article  CAS  Google Scholar 

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Acknowledgments

Thanks to Martin Enghoff (Copenhagen) and Nesrine Akkari (ZMUC) for helping in various ways to discover the new fungus species, first in a Copenhagen backyard. Thanks to David Koon-Bong Cheung (ZMUC) for photography. Thanks to Nesrine Akkari (now NMW), Göran Andersson (NMG), Dragan Antić (Belgrade), Pablo Barranco (Almeria), Jeannine Bortels (FUSAGx), Jerôme Constant (RBINS), Peter Decker (Görlitz), Laurent Delfosse (FUSAGx), Per Djursvoll (ZMUC), Jason Dunlop (MFN), Jean-Jacques Geoffroy MNHN), José Domingo Gilgado (Alcalá), Slobodan Makarov (Belgrade), Timo Pajonen (FMNH), Graham Proudlove (MM), Hans Reip (Jena), Pavel Stoev (Sofia), Henrik Sundberg (Uppsala) and Boyan Vagalinski (Sofia) for lending specimens under their care. The specimens provided by P. Barranco derive from a study partially supported by FEADER (EEC) and Consejeria del Medio Ambiente de la Junta de Andalucia (Spain), and thanks are also due to Grupo de Investigaciones Espeleológicas de Jérez (GIEX) for collecting host millipedes for T. pusillus. We are grateful to Walter Rossi (Univ. L’Aquila, Italy) for useful comments on an advanced manuscript draft.

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  1. Natural History Museum of Denmark (Zoological Museum), University of Copenhagen, Universitetsparken 15, DK-2100, København Ø, Denmark

    Henrik Enghoff

  2. Unitat de Botànica, Departament de Biologia Animal, de Biologia Vegetal i d’Ecologia, Facultat de Biociències, Universitat Autònoma de Barcelona, 08193-Bellaterra, Barcelona, Spain

    Sergi Santamaria

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Enghoff, H., Santamaria, S. Infectious intimacy and contaminated caves—three new species of ectoparasitic fungi (Ascomycota: Laboulbeniales) from blaniulid millipedes (Diplopoda: Julida) and inferences about their transmittal mechanisms. Org Divers Evol 15, 249–263 (2015). https://doi.org/10.1007/s13127-015-0208-8

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