Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter October 15, 2017

Natural occurrence of microsporidia infecting Lepidoptera in Bulgaria

Daniela Pilarska, Danail Takov, Miroslav Hyliš, Renate Radek, Ivan Fiala, Leellen Solter and Andreas Linde
From the journal Acta Parasitologica

Abstract

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.

Acknowledgments

The research was supported by the German Research Foundation (DFG), German Academic Exchange Service (DAAD), National Science Fund of Bulgaria, Project D)-02-251/2008.

References

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.2013.07.00710.1016/j.jip.2013.07.007Search in Google Scholar PubMed

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)Search in 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. 451–47010.1016/B978-0-12-386899-2.00015-4Search in Google 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. 10.1002/9781118395264.ch25Search in Google 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. 10.1086/303404Search in Google 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/12.6.54310.1093/bioinformatics/12.6.543Search in Google Scholar

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. 10.1016/j.jip.2004.07.006Search in Google 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.2005.11.00610.1016/j.jip.2005.11.006Search in Google Scholar PubMed

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. 10.3389/fmicb.2014.00112Search in Google Scholar PubMed

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. 10.1093/nar/gki198Search in Google Scholar PubMed

Kohler S.L., Hoiland W.K. 2001. Population regulation in an aquatic insect: The role of disease. Ecology, 82, 2294–2305. 10.1890/00129658(2001)082[2294:PRIAAI]2.0.CO;2Search in Google 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, 299–308Search in Google 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, 59–65Search in Google 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)Search in Google Scholar

Pilarska D. 1987. Study of microsporidia of some important lepidopteran species in South Western Bulgaria. Charles University, Prague, Ph.D. thesis, pp. 220Search in Google 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, 115–121Search in Google 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, 246–249Search in Google Scholar

Pilarska D. 1994. A microsporidian, Nosema carpocapsae Paillot, 1938 (Microspora, Nosematidae), a new parasite for Laspeyresia molesta Buscq (Lepidoptera, Tortricidae). Acta Parasitologica, 39, 62–63Search in Google 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, 253–257Search in Google 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, 109–113Search in Google Scholar

Pilarska D., Solter L., Danova E. 2000. Microsporidia in Lymantridae and Tortricidae from Bulgaria. Annual of Sofia University, 92, 65–68Search in Google 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, 37–3910.1046/j.1439-0280.2001.01007.xSearch in Google 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, 1–5Search in Google 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. 10.1016/j.jip.2014.09.007Search in Google Scholar PubMed

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

Richardson K.C., Jarett L., Finke E.H. 1960. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology, 35, 313–32510.3109/10520296009114754Search in Google Scholar PubMed

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, 1168–118510.1017/S0031182013000668Search in Google Scholar PubMed

Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. https://doi.org/10.1093/bioinformatics/btg18010.1093/bioinformatics/btg180Search in Google Scholar PubMed

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.1996.465010.1006/jipa.1996.4650Search in Google Scholar PubMed

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.2000.084510.1006/bcon.2000.0845Search in Google Scholar

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. 10.1016/j.jip.2010.04.009Search in Google Scholar PubMed

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, 221–26310.1016/B978-0-12-384984-7.00007-5Search in Google 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/btl44610.1093/bioinformatics/btl446Search in Google Scholar PubMed

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.2013.08.00510.1016/j.pt.2013.08.005Search in Google Scholar PubMed

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, 525–53910.1080/10635150117959Search in Google Scholar PubMed

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. 10.1111/j.1550-7408.2006.00108.xSearch in Google Scholar PubMed

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. 10.1128/9781555818227.ch4Search in Google Scholar

Received: 2017-5-22
Revised: 2017-8-16
Accepted: 2017-8-21
Published Online: 2017-10-15
Published in Print: 2017-12-20

© 2017 W. Stefański Institute of Parasitology, PAS