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The life cycle of Gregarina cuneata in the midgut of Tribolium castaneum and the effects of parasitism on the development of insects

Published online by Cambridge University Press:  19 January 2016

A.A.S. Gigliolli ,
A.H.F. Julio  and
H. Conte
A.A.S. Gigliolli*
Affiliation:
Departamento de Biotecnologia, Genética e Biologia Celular, Universidade Estadual de Maringá (UEM), Paraná, Brazil
A.H.F. Julio
Affiliation:
Departamento de Biotecnologia, Genética e Biologia Celular, Universidade Estadual de Maringá (UEM), Paraná, Brazil
H. Conte
Affiliation:
Departamento de Biotecnologia, Genética e Biologia Celular, Universidade Estadual de Maringá (UEM), Paraná, Brazil
*
*Author for correspondence Phone: +55 44 30114466/ +55 44 99846378 E-mail: adrianasinopolis@hotmail.com
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Abstract

Tribolium castaneum Herbst 1797 (Coleoptera: Tenebrionidae), an important pest of stored grains and byproducts, is naturally infected by Gregarina cuneata Stein 1848 (Apicomplexa: Gregarinidae). Changes in the life cycle of insects caused by the parasite development in the midgut were studied. Trophozoites, gamonts (solitary and associated), and gametocysts were present in the midgut of the insects. In young trophozoites, the apical region differentiated into an epimerite that firmly attached the parasite to the host epithelial cells. With maturation, trophozoites developed in gamonts that were associated with the initiation of sexual reproduction in the cell cycle, culminating in the formation of the spherical gametocyst. Morpho-functional analyses indicated that gregarines absorb nutrients from infected cells and can occlude the midgut as they develop. Consequently, nutritional depletion may interfere with the host's physiology, causing decreased growth, delayed development, and high mortality rates of the parasitized insects. These results suggest G. cuneata could be an important biological agent for controlling T. castaneum in integrated pest management programs.

Keywords

Tribolium castaneumGregarinesmorphologydevelopmentalmortalitycontrol biological
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 2 , April 2016 , pp. 258 - 267
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Copyright
Copyright © Cambridge University Press 2016 

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References

Agnew, P., Koella, J.C. & Michelakis, Y. (2000) Host life history responses to parasitism. Microbes and Infection 2, 891–896.Google Scholar
Ball, S.J., Cunningham, A.A., Clake, D. & Daszak, P. (1995) Septate gregarines associates with a disease of the hissing cockroach Gromphadorhina portentosa . Journal of Invertebrate Pathology 65, 311–312.CrossRefGoogle Scholar
Baudoin, J. (1969) On the ultrastructure of the anterior region of the gregarine Ancyrophora puytoraci . Protistologica 5, 431–439.Google Scholar
Bouwma, A.J., Howard, K.J. & Jeanne, R.L. (2005) Parasitism in a social wasp: effect of gregarines on foraging behaviour, colony productivity, and adult mortality. Behavioral Ecology Sociobiology 59, 222–233.Google Scholar
Brooks, W.M. & Jackson, J. (1990) Eugregarines: current status as pathogens, illustrated in corn rootworms. pp. 512–515 in Pinnock, D.E. (Ed.), International Colloquium on Invertebrate Pathology and Microbial Control. Adelaide, Australia.Google Scholar
Clopton, R.E. & Gold, R.E. (1995) Effects of pH on excystation in G. cuneata and Gregarina polymorpha (Eugregarinida: Gregarinidae). Journal of Eukaryotic Microbiology 42, 540–544.Google Scholar
Clopton, R.E. & Janovy, J.J.R. (1993) Developmental niche structure in the gregarine assemblage parasitizing Tenebrio molitor . Journal of Parasitology 79, 701–709.Google Scholar
Dunkel, F.V. & Boush, G.M. (1969) Effect of starvation on the black carpet beetle, Attagenus megatoma, infected with the eugregarine Pyxinia frenzeli . Journal of Invertebrate Pathology 14, 49–52.Google Scholar
Er, M.K. & Gokce, A. (2005) Effect of Diplocystis tipulae sherlock (Eugregarinida: Apicomplexa), a coelomic gregarine pathogen of tipulids, on the larval size of Tipula paludosa meigen (Tipulidae: Diptera). Journal of Invertebrate Pathology 89, 112–115.CrossRefGoogle ScholarPubMed
Gigliolli, A.A.S., Lapenta, A.S., Ruvolo-Takasusuki, M.C.C., Abrahão, J. & Conte, H. (2015) Morpho-functional characterization and esterase patterns of the midgut of T. castaneum Herbst, 1797 (Coleoptera: Tenebrionidae) parasitized by G. cuneata (Apicomplexa: Eugregarinidae). Micron 76, 68–78.Google Scholar
Gourbal, B.E.F., Righi, M., Petit, G. & Gabrion, C. (2001) Parasite-altered host behavior in the face of a predator: manipulation or not? Parasitological Research 87, 186–192.CrossRefGoogle ScholarPubMed
Harry, O.G. (1967) The effect of a eugregarine Gregarina polymorpha (Hammerschmidt) on the mealworm larva of Tenebrio molitor (L.). Journal of Eukaryotic Microbiology 14, 539–547.Google ScholarPubMed
Harry, O.G. (1970) Gregarines: their effect on the growth of the desert locust (Schistocerca gregaria). Nature 225, 964–966.CrossRefGoogle ScholarPubMed
Heintzelman, M.B. (2004) Actin and myosin in Gregarina polymorpha . Cell Motility and the Cytoskeleton 58, 83–95.Google Scholar
Hildebrand, H.F. (1976) Electron-microscopic investigation on evolution stages of trophozoite of Didymophyes gigantea (Sporozoa, Gregarinida). 1. Fine structure of protomerite and epimerite and relationship between host and parasite. Parasitology Research 49, 193–215.Google Scholar
Hoshide, K. (1979) Notes on the gregarines in Japan 10. Three new and seventeen aldeady known species of gregarines from Japanese Tenebrionidae. Bulletin of the Faculty of Education Yamaguchi University 29, 31–75.Google Scholar
Ishii, S. (1914) On four polycystid gregarines from the intestine of Tribolium ferrugineum F. Annotationes Zoologicae Japonenses 8, 435–441.Google Scholar
Johny, S., Muralirangan, M.C. & Sanjayan, K.P. (2000) Parasitization portencial of two cephaline gregarines, Leidyana Subramanii Pushkala and Muralirangan and Retractocephalus dhawanii sp. N. on the Tobacco Grasshopper, Atractomorpha crenulata (FB.). Journal of Orthoptera Research 9, 67–70.CrossRefGoogle Scholar
Junqueira, L.C.U. & Junqueira, L.M.M.S. (Eds) (1983) Técnicas básicas de citologia e histologia, pp. 123. São Paulo, Livraria e Editora Santos. Google Scholar
Lange, C.E. & Cigliano, M.M. (2004) The life cycle of Leidyana ampulla sp. n. (Apicomplexa: Eugregarinorida: Leidyanidae) in the grasshopper Ronderosia bergi (Stal) (Orthoptera: Acrididae: Melanoplinae). Acta Protozoologica 43, 81–87.Google Scholar
Lange, C. & Lord, J. (2011) Entomopathogenic protists. pp. 367–394 in Vega, F.E. & Kaya, H.K. (Eds) Insect Pathology. San Diego, Elsevier.Google Scholar
Lantova, L., Svobodova, M. & Volf, P. (2011) Effects of Psychodiella sergenti (Apicomplexa, Eugregarinorida) on its natural host Phlebotomus sergenti (Diptera, Psychodidae). Journal of Medical Entomology 48, 985–990.CrossRefGoogle ScholarPubMed
Lefèvre, T., Lebarbenchon, C., Gauthier-Clerc, M., Poulin, R. & Thomas, F. (2009) The ecological significance of manipulative parasites. Trends in Ecological Evolution 24, 41–48.CrossRefGoogle ScholarPubMed
Lopes, R.B. & Alves, S. (2005) Effect of Gregarina sp. parasitism on the susceptibility of Blattella germanica to some control agents. Journal Invertebrate Pathology 88, 261–264.CrossRefGoogle ScholarPubMed
Lord, J.C. & Omoto, C.K. (2012) Eugregarines reduce susceptibility of the hide beetle, Dermestes maculatus, to apicomplexan pathogens and retard larval development. Journal of Invertebrate Pathology 111, 186–188.CrossRefGoogle ScholarPubMed
Lucarotti, C.J. (2000) Cytology of Leidyana canadensis (Apicomplexa: Eugregarinida) in Lambdina fiscellaria fiscellaria larvae (Lepidoptera: Geometridae). Journal of Invertebrate Pathology 75, 117–125.CrossRefGoogle ScholarPubMed
MacMillan, W.G. (1973) Gregarine attachment organelles – structure and permeability of an interspecific cell junction. Parasitology 66, 207–214.CrossRefGoogle Scholar
R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org/ Google Scholar
Rodriguez, Y., Omoto, C.K. & Gomulkiewicz, R. (2007) Individual and population effects of Eugregarine, Gregarina niphandrodes (Eugregarinida: Gregarinidae), on Tenebrio molitor (Coleoptera: Tenebrionidae). Environmental Entomology 36, 689–693.Google Scholar
Ruhl, H. (1976) Contribution to the physiology of movement of gregarines: elements of movement, movement modes. Zeitschrift für Parasitenkunde 48, 199–214.Google Scholar
Schawang, J.E. & Janovy, J.J.R. (2001) The response of Gregarina niphandrodes (Apicomplexa: Eugregarinida: Septatina) to host starvation in Tenebrio molitor (Coleoptera: Tenebrionidae) adults. Journal of Parasitology 87, 600–605.Google Scholar
Schewiakoff, W. (1894) Uber die Ursache der fortschreitenden Bewegung der Gregarinen. Zeitschrift für wissenschaftliche Zoologie 58, 340–354.Google Scholar
Schreurs, J. & Janovy, J.J.R. (2008). Gregarines on a diet: the effects of host Starvation on Gregarina confusa Janovy et al., 2007 (Apicomplexa: Eugregarinida) in Tribolium destructor Uyttenboogaart, 1933 (Coleoptera: Tenebrionidae) Larvae. Journal of Parasitology 94, 567–570.Google Scholar
Schrevel, J. (1972) Polysaccharides of cell-surface of gregarines (Protozoa Parasites). 1. Ultrastructure and cytochemistry. Journal of Microscopy 15, 21–40.Google Scholar
Schrevel, J. & Philippe, M. (1993) The gregarines. pp. 133–245 in Kreier, J.P. (Ed.) Parasitic Protozoa. San Diego, Academic Press.Google Scholar
Schwalbe, C.P. & Baker, J.E. (1976) Nutrient reserves in starving black carpet beetle larvae infected with the eugregarine Pyzinia frenzeli . Journal of Invertebrate Pathology 28, 11–15.Google Scholar
Scudeler, E.L. & Santos, D.C. (2013) Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae). Micron 44, 125–132.CrossRefGoogle ScholarPubMed
Smiderle, O. (2007) Manejo integrado de pragas de grãos armazenados: identificação e controle. Artigo em Hypertexto. Available online at: http://www.infobibos.com/artigos/2007_2/pragasgraos/Index.htm (acesso em 06/03/2008).Google Scholar
Smith, A.J., Cook, T.J. & Lutterschmidt, W.I. (2007) Effects of temperature on the development of Gregarina cubensis (Apicomplexa: Eugregarinida) parasitizing Blaberus discoidalis (Blattaria: Blaberidae). Journal of Parasitology 93, 583–588.CrossRefGoogle ScholarPubMed
Talluri, M.V. & Dallai, R. (1983) Freeze-fracture study of the gregarine trophozoite: II. Evidence of ‘‘rosette’’ organization on cytomembranes in relation with micropore structure. Bollettino di Zoologia 50, 247–256.Google Scholar
Thomas, A.M. & Rudolf, V.H.W. (2010) Challenges of metamorphosis in invertebrate hosts: maintaining parasite resistance across life-history stages. Ecological Entomology 35, 200–205.CrossRefGoogle Scholar
Toso, M.A. & Omoto, C.K. (2007) Ultrastructure of the Gregarina niphandrodes nucleus through stages from unassociated trophozoites to gamonts in syzygy and the syzygy junction. Journal of Parasitology 93, 479–484.CrossRefGoogle ScholarPubMed
Valigurová, A. (2012) Sophisticated adaptations of G. cuneata (Apicomplexa) feeding stages for Epicellular parasitism. PLoS ONE 7, 1–11.Google Scholar
Valigurová, A. & Koudela, B. (2005) Fine structure of trophozoites of the gregarine Leidyana ephestiae (Apicomplexa: Eugregarinida) parasitic in Ephestia kuehniella larvae (Lepidoptera). European Journal of Protistology 41, 209–218.Google Scholar
Valigurová, A. & Koudela, B. (2008) Morphological analysis of the cellular interactions between the eugregarine Gregarina garnhami (Apicomplexa) and the epithelium of its host, the desert locust Schistocerca gregaria . European Journal of Protistology 44, 197–207.CrossRefGoogle ScholarPubMed
Valigurová, A., Hofmannova, L., Koudela, B. & Vavra, J. (2007) An ultrastructural comparison of the attachment sites between Gregarina steini and Cryptosporidium muris. Journal of Eukaryotic Microbiology 54, 495–510.Google Scholar
Valigurová, A., Jirku, M., Koudela, B., Gelnar, M., Modry, D. & Slapeta, J. (2008) Cryptosporidia: epicellular parasites embraced by the host cell membrane. International Journal for Parasitology 38, 913–922.Google Scholar
Valigurová, A., Michalkova, V. & Koudela, B. (2009) Eugregarine trophozoite detachment from the host epithelium via epimerite retraction: fiction or fact? International Journal for Parasitology 39, 1235–1242.CrossRefGoogle ScholarPubMed
Valigurová, A., Vaškovicová, N., Musilová, N. & Schrével, J. (2013) The enigma of eugregarine epicytic folds: where gliding motility originates? Frontiers in Zoology 10, 2–27.CrossRefGoogle ScholarPubMed
Vivier, E. (1968) L'organisation ultrastructurale corticale de la Gregarine Lecudina pellucida; ses rapports avec l'alimentation et la locomotion. Journal of Protozoology 15, 230–246.Google Scholar
Walker, M.H., Mackenzie, C., Bainbridge, S.P. & Orme, C. (1979) A study of the structure and gliding movement of Gregarina garnhami . Journal of Protozoology 26, 566–574.Google Scholar