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Acta Parasitologica

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Volume 62, Issue 4


Natural occurrence of microsporidia infecting Lepidoptera in Bulgaria

Daniela Pilarska
  • Corresponding author
  • New Bulgarian University, Department of Natural Sciences, Sofia, Bulgaria
  • Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Danail Takov
  • Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Miroslav Hyliš
  • Laboratory of Electron Microscopy, Faculty of Science, Charles University in Prague, Prague, Czech Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Renate Radek / Ivan Fiala
  • Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic
  • Department of Parasitology, Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Leellen Solter
  • Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Illinois, USA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Andreas Linde
Published Online: 2017-10-15 | DOI: https://doi.org/10.1515/ap-2017-0104


We examined 34 lepidopteran species belonging to 12 families to determine presence and prevalence of microsporidian pathogens. The insects were collected from May 2009 to July 2012 from 44 sites in Bulgaria. Nosema species were isolated from Archips xylosteana, Tortrix viridana, Operophtera brumata, Orthosia cerasi, and Orthosia cruda. Endoreticulatus sp. was isolated from Eilema complana. The prevalence of all isolates in their hosts was low and ranged from 1.0% to 5.3%. Phylogenetic analyses of the new isolates based on SSU rDNA are presented.

Keywords: Biogeography; biological control; entomopathogens


  • Andreadis T.G., Takaoka H., Otsuka Y., Vossbrinck C.R. 2013. Morphological and molecular characterization of a microsporidian parasite, Takaokaspora nipponicus n. gen., n. sp. from the invasive rock pool mosquito, Ochlerotatus japonicus japonicus. Journal of Invertebrate Pathology, 114, 161–72. http://dx.doi.org/10.1016/j.jip.2013.07.007PubMedCrossrefWeb of Science

  • Atanasov, A. 1982. Study on the distribution of diseases and their role for the reduction of codling moth population density of Laspeyresia pomonella. Probl. Biol. Borba Vredit. Selsko Gorsko Stop., 3, 298. (In Bulgarian)Google Scholar

  • Becnel J.J. 2012. Complementary techniques: preparations of entomopathogens and diseased specimens for more detailed study using microscopy. In: (Ed. L.A. Lacey), Manual of Techniques in Invertebrate Pathology. San Diego, Elsevier, pp. 451–470Google Scholar

  • Bjørnson S., Oi D. 2014. Microsporidia biological control agents and pathogens of beneficial insects. In: (Eds: L.M. Weiss and J.J. Becnel), Microsporidia: Pathogens of Opportunity, 1. ed. John Wiley & Sons, Inc., pp. 635–670. CrossrefGoogle Scholar

  • Ebert, D., Lipsitch, M., Mangin, K.L. 2000. The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. The American Naturalist, 156, 459–477. CrossrefGoogle Scholar

  • Galtier N., Gouy M., Gautier C. 1996. SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences, 12, 543–548. https://doi.org/10.1093/bioinformatics/12.6.543

  • Goertz D., Pilarska D., Kereselidze M., Solter L., Linde A. 2004. Studies on the impact of two Nosema isolates from Bulgaria on the gypsy moth (Lymantria dispar L.). Journal of Invertebrate Pathology, 87, 105–113. CrossrefGoogle Scholar

  • Hylis, M., Pilarska, D. K., Obornik, M., Vavra, J., Solter, L., Weiser, J., Linde, A., McManus, M. 2006. Nosema chrysorrhoeae n. sp. (Microsporidia), isolated from browntail moth (Euproctis chrysorrhoea L.) (Lepidoptera, Lymantriidae) in Bulgaria: Characterization and phylogenetic relationships. Journal of Invertebrate Pathology, 91, 105–114. DOI:10.1016/j.jip.2005.11.006CrossrefPubMedGoogle Scholar

  • Karpov S.A., Mamkaeva M.A., Aleoshin V.V., Nassonova E., Lilje O., Gleason F.H. 2014. Morphology, phylogeny, and ecology of the aphelids (Aphelidae, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Frontiers in Microbiology 5, Article 112. CrossrefPubMedGoogle Scholar

  • Katoh K., Kuma K., Toh H., Miyata, T. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511–518. CrossrefPubMedGoogle Scholar

  • Kohler S.L., Hoiland W.K. 2001. Population regulation in an aquatic insect: The role of disease. Ecology, 82, 2294–2305. CrossrefGoogle Scholar

  • Malysh J.M., Tokarev Y.S., Sitnicova N.V., Martemyanov V.V., Frolov A.N., Issi I.V. 2013. Tubulinosema pyraustae sp.n. (Microsporidia: Tubulinosematidae) from the beet webworm Pyrausta (Loxostege) sticticalis L. (Lepidoptera: Crambidae) in Western Siberia. Acta Protozoologica, 52, 299–308Google Scholar

  • Mirchev P., Penev D., Ovcharov D. 1987. Factors determining the population number of the gypsy moth (Lymantria dispar L.). Gorskostopanska Nauka (Forest Science), 24, 59–65Google Scholar

  • Panayotov P., Zashev B., Cankov G., Grigorova R. 1960. Nosematosis of the gypsy moth (Nozematozata po gabotvorkata). Izv. Nauch. Inst. Gor., 6, 201. (In Bulgarian)Google Scholar

  • Pilarska D. 1987. Study of microsporidia of some important lepidopteran species in South Western Bulgaria. Charles University, Prague, Ph.D. thesis, pp. 220Google Scholar

  • Pilarska D., Vavra J. 1991. Morphology and development of Nosema serbica Weiser, 1963 (Microspora, Nosematidae), parasite of the gypsy moth Lymantria dispar (Lepidoptera, Lymantriidae). Folia Parasitologica, 38, 115–121Google Scholar

  • Pilarska D. 1993. Investigations on the occurrence and biology of the microsporidium Nosema carpocapsae Paillot a parasite of the codling moth Cydia pomonella (Lepidoptera: Tortricidae). In: Proceedings of the Second National Scientific Conference of Entomology, 25–27.10.1993, Sofia, Bulgaria, 246–249Google Scholar

  • Pilarska D. 1994. A microsporidian, Nosema carpocapsae Paillot, 1938 (Microspora, Nosematidae), a new parasite for Laspeyresia molesta Buscq (Lepidoptera, Tortricidae). Acta Parasitologica, 39, 62–63Google Scholar

  • Pilarska D. 1995. First record a microsporidian infection of Lobesia botrana (Den a Schiff) (Lepidoptera: Tortricidae) in Bulgaria. In: Proceedings of the Third National Scientific Conference of Entomology, 18–20.09.1995, Sofia, 253–257Google Scholar

  • Pilarska D., Solter L., Maddox J., McManus M. 1998. Microsporidia from gypsy moth (Lymantria dispar L.) populations in Central and Western Bulgaria. Acta Zoologica Bulgarica, 50, 109–113Google Scholar

  • Pilarska D., Solter L., Danova E. 2000. Microsporidia in Lymantridae and Tortricidae from Bulgaria. Annual of Sofia University, 92, 65–68Google Scholar

  • Pilarska D., Linde A., Goertz D., McManus M., Solter L., Bochev N., Rajkova M. 2001. First report on the distribution of microsporidian infections of browntail moth (Euproctis chrysorrhoea L.) populations in Bulgaria. Journal of Pest Science (Anzeiger für Schädlingskunde), 74, 37–39CrossrefGoogle Scholar

  • Pilarska D., Linde A., Solter L., Takov D., McManus M., Goertz D. 2002. Ultrastructure characteristic of a Nosema sp. (Microsporidia) from a Bulgarian population of Euproctis chrysorrhoea L. (Lepidoptera). Acta Parasitologica, 47, 1–5Google Scholar

  • Pilarska D., Radek R., Huang W.F., Takov D.I., Linde A., Solter A. 2015. Review of the genus Endoreticulatus (Microsporidia, Encephalitozoonidae) with description of a new species isolated from the grasshopper Poecilimon thoracicus (Tettigoniidae) and transfer of Microsporidium itiiti Malone to the genus. Journal of Invertebrate Pathology, 124, 23–30. CrossrefWeb of ScienceGoogle Scholar

  • Rambaut, A., Drummond, A.J., 2007. Tracer v1.4: MCMC trace analyses tool. Available: http://beast.bio.ed.ac.uk/Tracer. Accessed 29 November 2008

  • Richardson K.C., Jarett L., Finke E.H. 1960. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology, 35, 313–325CrossrefPubMedGoogle Scholar

  • Rode N.O., Landes J., Lievens E.J.P., Flaven E., Segard A., Jabbour-Zahab R., Michalakis Y., Agnew P., Vivares C.P., Lenormand T. 2013. Cytological, molecular and life cycle characterization of Anostracospora rigaudi n. g., n. sp. and Enterocytospora artemiae n. g., n. sp., two new microsporidian parasites infecting gut tissues of the brine shrimp Artemia. Parasitology, 140, 1168–1185CrossrefWeb of ScienceGoogle Scholar

  • Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. https://doi.org/10.1093/bioinformatics/btg180PubMedCrossref

  • Solter L.F., Maddox J.V., McManus M.L. 1997. Host specificity of microsporidia (Protista: Microspora) from European populations of Lymantria dispar (Lepidoptera: Lymantriidae) to indigenous North American Lepidoptera. Journal of Invertebrate Pathology, 69, 135–150. https://doi.org/10.1006/jipa.1996.4650CrossrefPubMed

  • Solter L., Pilarska D., Vossbrinck C. 2000. Host specificity of microsporidia pathogenic to forest Lepidoptera. Biological Control, 19, 48–56. http://dx.doi.org/10.1006/bcon.2000.0845Crossref

  • Solter L., Pilarska D., McManus M., Zubrik M., Patocka J., Huang, W.F., Novotny J. 2010. Host specificity of microsporidia pathogenic to the gypsy moth, Lymantria dispar (L.): Field studies in Slovakia. Journal of Invertebrate Pathology, 105, 1–10. CrossrefPubMedWeb of ScienceGoogle Scholar

  • Solter L.F., Becnel J.J., Oi D.H. 2012. Microsporidian entomopathogens. In: (Eds: F.E. Vega and H.K. Kaya), Insect Pathology, Second Edition. San Diego, Elsevier, 221–263Google Scholar

  • Stamatakis A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690. DOI:10.1093/bioinformatics/btl446PubMedCrossrefGoogle Scholar

  • Stentiford G.D., Feist S.W., Stone D.M., Bateman K.S., Dunn A.M. 2014. Microsporidia: Diverse, dynamic, and emergent pathogens in aquatic systems. Trends in Parasitology, 29, 567–578. http://dx.doi.org/10.1016/j.pt.2013.08.005Web of Science

  • Swofford D. L., Waddell P. J., Huelsenbeck J. P., Foster P. G., Lewis P. O., Rogers J. S. 2001. Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Systematic Biology, 50, 525–539CrossrefPubMedGoogle Scholar

  • Vavra, J., Hylis M., Vossbrinck, C., Pilarska, D., Linde, A., Weiser, J., et al. 2006. Vairimorpha disparis n. comb. (Microsporidia: Burenellidae): A redescription and taxonmic revision of Thelohania disparis Timofejeva 1956, a microsporidian parasite of the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae). Journal of Eukaryotic Microbiology, 53, 292–304. CrossrefGoogle Scholar

  • Weiss L.M., Vossbrinck C.R. 1999. Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the Microsporidia. In: (Eds: M. Wittner and L.M. Weiss), The Microsporidia and Microsporidiosis. Washington, D.C., ASM Press, 129–171. CrossrefGoogle Scholar

About the article

Received: 2017-05-22

Revised: 2017-08-16

Accepted: 2017-08-21

Published Online: 2017-10-15

Published in Print: 2017-12-20

Citation Information: Acta Parasitologica, Volume 62, Issue 4, Pages 858–869, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2017-0104.

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