Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-24T11:39:55.177Z Has data issue: false hasContentIssue false

The effect of Blastocrithidia triatomae (Trypanosomatidae) on the midgut of the reduviid bug Triatoma infestans

Published online by Cambridge University Press:  06 April 2009

C. Jensen
Affiliation:
Institut für Biologie I (Zoologie), Albert-Ludwigs-Universität, Albertstrasse 21a, D-7800 Freiburg, Federal Republic of Germany
G. A. Schaub
Affiliation:
Institut für Biologie I (Zoologie), Albert-Ludwigs-Universität, Albertstrasse 21a, D-7800 Freiburg, Federal Republic of Germany
D. H. Molyneux
Affiliation:
Department of Biological Sciences, University of Salford, Salford M5 4WT, England

Summary

The pathogenic flagellate Blastocrithidia triatomae disrupts the digestion of Triatoma infestans; the midgut ultrastructure of bugs infected with the flagellate and of uninfected bugs is compared. Third or fourth instar larvae were dissected either unfed or 1 week after feeding.In all uninfected bugs extracellular membrane layers (e.m.l.) covered the apical microvillar border of the epithelial cells. Some midgut regions of bugs infected with B. triatomae appeared normal but often adjacent cells showed pathological effects. In affected cells the e.m.l. and the microvilli and finally the cells themselves were reduced or destroyed. Correlated with these observations of pathogenicity the method of attachment of parasites changed. When the e.m.l. were present only rarely were flagella found, but on extracellular membrane-free cells B. triatomae attached by flagellar enlargement to the microvillar border or, if this was reduced, to the apical host cell membrane. No hemidesmosome-like plaques were found at the attachment site. Although some flagella were inserted into the apical region of the cells no intracellular flagellates were observed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ayala, S. C. (1971). Trypanosomes in wild California sandflies, and extrinsic stages of Trypanosoma bufophlebotomi. Journal of Protozoology 18, 433–6.CrossRefGoogle ScholarPubMed
Baker, J. R. (1956). Studies on Trypanosoma avium Danilewsky 1885. III. Life-cycle in vertebrate and invertebrate hosts. Parasitology 46, 335–51.CrossRefGoogle ScholarPubMed
Bauer, P. G. (1981). Ultrastrukturelle und physiologische Aspekte des Mitteldarms von Rhodnius prolixus Stål (Insecta, Heteroptera), Dissertation, Universität Basel.Google Scholar
Billingsley, P. F. & Downe, A. E. R. (1983). Ultrastructural changes in posterior midgut cells associated with blood feeding in adult female Rhodnius prolixus Stål (Hemiptera: Reduviidae). Canadian Journal of Zoology 61, 2574–86.CrossRefGoogle Scholar
Billingsley, P. F. & Downe, A. E. R. (1985). Cellular localisation of aminopeptidase in the midgut of Rhodnius prolixus Stål (Hemiptera: Reduviidae) during blood digestion. Cell and Tissue Research 241, 421–8.CrossRefGoogle Scholar
Billingsley, P. F. & Downe, A. E. R. (1986). The surface morphology of the midgut cells of Rhodnius prolixus Stål (Hemiptera: Reduviidae) during blood digestion. Acta Tropica 43, 355–66.Google ScholarPubMed
Böker, C. A. & Schaub, G. A. (1984). Scanning electron microscopic studies of Trypanosoma cruzi in the rectum of its vector Triatoma infestans. Zeitschrift für Parasitenkunde 70, 459–69.CrossRefGoogle ScholarPubMed
Evans, D. A. & Ellis, D. S. (1983). Recent observations on the behaviour of certain trypanosomes within their insect hosts. Advances in Parasitology 22, 142.CrossRefGoogle ScholarPubMed
Feng, L. C. (1951). The role of the peritrophic membrane in Leishmania and Trypanosoma infections of sandflies. Peking Natural History Bulletin 19, 327–34.Google Scholar
Hecker, H. & Moloo, S. K. (1981). Influence of Trypanosoma (Trypanozoon) brucei infection on the fine structure of midgut cells of Glossina m. morsitans. Parasitology 82, (4), 106–7.Google Scholar
Kaddu, J. B. & Mutinga, M. J. (1981). Leishmania in Kenyan phlebotomine sandflies — I. Leishmania aethiopica in the midgut of naturally infected Phlebotomus pedifer. Insect Science and Application 2, 245–50.Google Scholar
Kaddu, J. B. & Mutinga, M. J. (1983). Vector—parasite relationships: the effect of Trypanosoma (Nannomonas) congolense on Glossina pallidipes. Annals of Tropical Medicine and Parasitology 77, 315–20.CrossRefGoogle ScholarPubMed
Killick-Kendrick, R., Lainson, R., Leaney, A. J., Ward, R. D. & Shaw, J. J. (1977). Promastigotes of Leishmania b. braziliensis in the gut wall of a natural vector, Psychodopygus wellcomei. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 381.Google Scholar
Killick-Kendrick, R., Molyneux, D. H. & Ashford, R. W. (1974). Leishmania in phlebotomid sandflies. I. Modifications of the flagellum associated with attachment to the mid-gut and oesophageal valve of the sandfly. Proceedings of the Royal Society London, B 187, 409–19.Google Scholar
Kramer, J. P. (1963). Pathogens of vertebrates and plants as pathogens of their acarine and insect vectors, In Insect Pathology, vol. 1 (ed. Steinhaus, E. A.), pp. 251272. New York: Academic Press.CrossRefGoogle Scholar
Langley, P. A. (1981). Digestion in haematophagous arthropods. Parasitology 82, (4), 95116.Google Scholar
Lipa, J. J. (1963). Infections caused by Protozoa other than Sporozoa. In Insect Pathology, vol. 2 (ed. Steinhaus, E. A.), pp. 335361. New York: Academic Press.CrossRefGoogle Scholar
Mehlhorn, H., Schaub, G. A., Peters, W. & Haberkorn, A. (1979). Electron microscopic studies on Blastocrithidia triatomae Cerisola et al. 1971 (Trypanosomatidae). Tropenmedizin und Parasitologie 30, 289300.Google ScholarPubMed
Molyneux, D. H. (1977). Vector relationships in the Trypanosomatidae. Advances in Parasitology 15, 182.CrossRefGoogle ScholarPubMed
Molyneux, D. H. (1983). Host—parasite relationships of Trypanosomatidae in vectors. In Current Topics in Vector Research, vol. 1 (ed. Harris, K. F.), pp. 117148. New York: Praeger Publishers.Google Scholar
Molyneux, D. H., Ryan, L., Lainson, R. & Shaw, J. J. (1986). The Leishmania-sandfly interface. In Leishmania: Taxonomie et Phylogenèse. Applications Eco-épidémiologiques, (Coll. Int. CNRS/INSERM, 1984) pp. 311324.Google Scholar
Molyneux, D. H., Wallbanks, K. R. & Ingram, G. A. (1987). Trypanosomatid—vector interfaces — in vitro studies on parasite substrate interactions. In Host—Parasite Cellular and Molecular Interactions in Protozoal Infections. NATO ASI Series, vol. H11 (ed. Chang, K.-P. & Snary, D.), pp. 387396. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Mungomba, L. M., Molyneux, D. H. & Wallbanks, K. R. (1989). Host—parasite relationship of Trypanosoma corvi in Ornithomyia avicularia. Parasitology Research 75, 167–74.CrossRefGoogle ScholarPubMed
Peters, W. (1982). Fine structure and permeability of peritrophic membranes in insects. In Parasites — Their World and Ours, Proceedings of the 5th International Congress of Parasitology, Toronto, 1982 (ed. Mettrick, D. F. & Desser, S. S.), pp. 9698. Amsterdam: Elsevier.Google Scholar
Reduth, D., Schaub, G. A. & Pudney, M. (1989). Cultivation of Blastocrithidia triatomae (Trypanosomatidae) on a cell line of its host Triatoma infestans (Reduviidae). Parasitology 98, 387–93.CrossRefGoogle ScholarPubMed
Schaub, G. A. (1988). Developmental time and mortality in larvae of the reduviid bugs Triatoma infestans and Rhodnius prolixus after coprohagic infection with Blastocrithidia triatomae (Trypanosomatidae). Journal of Invertebrate Pathology 51, 2331.CrossRefGoogle ScholarPubMed
Schaub, G. A. (1989). Trypanosoma cruzi: quantitative studies of development of two strains in small intestine and rectum of the vector Triatoma infestans. Experimental Parasitology 68, 260–73.CrossRefGoogle ScholarPubMed
Schaub, G. A. & Böker, C. A. (1986). Scanning electron microscopic studies of Blastocrithidia triatomae (Trypanosomatidae) in the rectum of Triatoma infestans (Reduviidae). Journal of Protozoology 33, 266–70.CrossRefGoogle Scholar
Schaub, G. A. & Breger, B. (1988). Pathological effects of Blastocrithidia triatomae (Trypanosomatidae) on the reduviid bugs Triatoma sordida, T. pallidipennis and Dipetalogaster maxima after coprophagic infection. Medical and Veterinary Entomology 2, 309–18.CrossRefGoogle ScholarPubMed
Schaub, G. A. & Lösch, P. (1989). Parasite/host interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans: Influence of starvation of the bug. Annals of Tropical Medicine and Parasitology 83, 215–23.CrossRefGoogle ScholarPubMed
Schaub, G. A. & Schnitker, A. (1988). Influence of Blastocrithidia triatomae (Trypanosomatidae) on the reduviid bug Triatoma infestans: Alterations of the Malpighian tubules. Parasitology Research 75, 8897.CrossRefGoogle ScholarPubMed
Schwarzenbach, M. A. (1987). Elektronenmikroskopische Untersuchungen zur Entwicklung von Trypanosoma (Herpetosoma) rangeli Tejera 1920 (Protozoa, Kinetoplastida) in seinem Überträger, Rhodnius prolixus Stal 1859 (Insecta, Heteroptera). Dissertation, Universität Basel.Google Scholar
Shaw, J. J. (1981). The behaviour of Endotrypanum schaudinni (Kinetoplastida: Trypanosomatidae) in three species of laboratory-bred neotropical sandflies (Diptera: Psychodidae) and its influence on the classification of the genus Leishmania. In Parasitological Topics (ed. Canning, E. U.), pp. 232241, Lawrence: Allen Press.Google Scholar
Terra, W. R., Ferreira, C. & De Bianchi, A. G. (1979). Distribution of digestive enzymes among the endo-and ectoperitrophic spaces and midgut cells of Rhynchosciara and its physiological significance. Journal of Insect Physiology 25, 487–94.CrossRefGoogle Scholar
Tetley, L. & Vickerman, K. (1985). Differentiation in Trypanosoma brucei: host—parasite cell junctions and their persistence during acquisition of the variable antigen coat. Journal of Cell Science 74, 119.CrossRefGoogle ScholarPubMed
Tieszen, K., Heywood, P. & Molyneux, D. H. (1983). Ultrastructure and host—parasite association of Blastocrithidia gerridis in the ventriculus of Gerris odontogaster (Gerridae: Hemiptera). Canadian Journal of Zoology 61, 1900–9.CrossRefGoogle Scholar
Tieszen, K. L., Molyneux, D. H. & Abdel-Hafez, S. K. (1986). Host—parasite relationships of Blastocrithidia familiaris in Lygaeus pandurus Scop. (Hemiptera: Lygaeidae). Parasitology 92, 112.CrossRefGoogle Scholar
Watkins, R. (1971). Histology of Rhodnius prolixus infected with Trypanosoma rangeli. Journal of Invertebrate Pathology 17, 5966.CrossRefGoogle ScholarPubMed