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Polychromophilus murinus: a malarial parasite of bats: life-history and ultrastructural studies

Published online by Cambridge University Press:  06 April 2009

R. A. Gardner  and
D. H. Molyneux
R. A. Gardner
Affiliation:
Department of Biological Sciences, University of Salford, Salford M5 4WT
D. H. Molyneux
Affiliation:
Department of Biological Sciences, University of Salford, Salford M5 4WT
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Summary

Polychromophilus murinus, a malaria parasite of Chiroptera is reported from Myotis daubentoni in England. The vector was suspected to be the ectoparasitic Nycteribiid fly, Nycteribia kolenatii. N. kolenatii collected from wild-caught M. daubentoni were found to have oocysts on the midgut and sporozoites in the salivary glands. Wild-caught N. kolenatii were maintained on two wild-caught M. daubentoni harbouring heavy (patent) infections of P. murinus; both oocysts and sporozoites were found in these flies. The mature oocysts measured 52–71 μm in diameter. Sporozoites were straight or slightly crescentic and had a mean length of 7·4 μm. Electron microscopy of immature and mature oocysts revealed a morphology similar to that of malaria parasites. Sporozoites were also similar in structure to Plasmodium sporozoites and were found in the epithelial cells of the salivary gland and within the lumen; a cytostome was present and transverse sections revealed 21 microtubules arranged evenly around the periphery. Sporozoites were observed within the basement membrane of the salivary gland of N. kolenatii; such sporozoites appeared to be penetrating the gland, a process hitherto not described in malaria parasites. Rickettsia-like bodies were found within the cytoplasm of the epithelial cells of the salivary gland. Exflagellation of microgametocytes was achieved. An ultrastructural study of the gametocytes revealed a structure similar to that described in other Haemoproteidae. A common feature of infected erythrocytes was a projecting erythrocyte membrane. Attempts to find schizogony in impression smears and sections of tissues of two infected M. daubentoni were not successful.

Type
Research Article
Information
Parasitology , Volume 96 , Issue 3 , June 1988 , pp. 591 - 605
Copyright
Copyright © Cambridge University Press 1988

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References

REFERENCE

Aikawa, N., (1977). Variations in structure and function during the life cycle of malarial parasites. Bulletin of the World Health Organization 55, 139–56.Google Scholar
Aikawa, M., Huff, C. G., & Sprinz, H., (1969). Comparative fine structure of gametocytes of avian, reptilian, and mammalian malaria parasites. Journal of Ultrastructural Research 26, 316–31.CrossRefGoogle Scholar
Aikawa, M., & Sterling, C. R., (1974). Intracellular Parasitic Protozoa. New York and London: Academic Press.Google Scholar
Bannister, L. H., Butcher, G. A., & Mitchell, G. H., (1977). Recent advances in understanding the invasion of erythrocytes by merozoites of Plasmodium knowlesi. Bulletin of the World Health Organization 55, 163–9.Google Scholar
Boulard, Y., Landau, I., Miltgen, F., Baccam, D., & Humphrey-Smith, I., (1985). Observations ultrastructurales sur la sporogonie d' Hepatocystis levinei, Haemoprotéidé, parasite de chiroptères Australiens chez Culicoides nubeculosus. Protistologica 21, 93–105.Google Scholar
Coles, A. C., (1914). Blood parasites found in mammals, birds and fishes in England. Parasitology 7, 17–61.CrossRefGoogle Scholar
Corradetti, A., (1936). Alcuni protozoi parassiti di Nycteribiidae del genere Listropoda. Annales di Igiene 46, 444–8.Google Scholar
Corradetti, A., Verlini, F., Palmieri, C., Neri, I., & Rostinolla, M., (1961). Studi su Polychromophilus melanipherus Dionisi, 1899, e su Polychromophilus murinus Dionisi, 1899. Parassitologia 3, 71–6.Google Scholar
Davies, E. E., Howells, R. E., & Venters, D., (1971). Microbial infections associated with plasmodial development in Anopheles stephensi. Annals of Tropical Medicine and Parasitology 65, 403–8.CrossRefGoogle ScholarPubMed
Desser, S. S., (1972). Gametocyte maturation, exflagellation and fertilization in Parahaemoproteus ( = Haemoproteus) velans (Coatney and Roudabush) (Haemosporidia: Haemoproteidae): an ultrastructural study. Journal of Protozoology 19, 287–96.CrossRefGoogle Scholar
Dew, B. B., & Mcmillan, (1970). Seasonal variation of Polychromophilus melanipherus (Sporozoa: Haemoproteidae) in the bent-winged bat Miniopterus schreibersi (Chiroptera) in New South Wales. Parasitology 61, 161–6.Google Scholar
Dionisi, A., (1899). La malaria di alcuni specie di pipistrelli. Atti delta Societa per gli Studi Malaria 1, 133–73.Google Scholar
Ellis, D. S., Evans, D. A., & Stamford, S., (1980). The penetration of the salivary glands of Rhodnius prolixus by Trypanosoma rangeli. Zeitschrift für Parasitenkunde 62, 63–74.Google Scholar
Gardner, R. A., (1986). Studies on the Haematozoa of British Bats. Ph.D. thesis, University of Salford, 214 pages.Google Scholar
Gardner, R. A., Molyneux, D. H., & Stebbings, R. E., (1987). Studies on the prevalence of Haematozoa of British bats. Mammal Review 17, 75–80.CrossRefGoogle Scholar
Garnham, P. C. C., (1966). Malaria Parasites and other Haemosporidia. Oxford: Blackwell Scientific Publications.Google Scholar
Garnham, P. C. C., (1973). The zoogeography of Polychromophilus and description of a new species of a gregarine (Lankesteria galliardi). Annales de Parasitologie Humaine et Comparée 48, 231–12.CrossRefGoogle ScholarPubMed
Garnham, P. C. C., (1980). Malaria in its various vertebrate hosts. In Malaria (ed. Kreier, J. P.) vol. 1, pp. 95–144. London: Academic Press.Google Scholar
Hutson, A. M., (1984). Keds, fiat-flies and bat-flies. Diptera, Hippoboscidae and Nycteribiidae. Handbook for the Identification of British Insects, vol. 10, Part 7, Royal Entomological Society London.Google Scholar
Kass, L., Willerson, D., Riekmann, K. H., Carson, P. G., & Becker, R. P., (1971). Plasmodium falciparum gametocytes. Electron microscope observations on material obtained by a new method. American Journal of Tropical Medicine and Hygiene 20, 187–94.Google Scholar
Kilejian, A., & Jensen, J. B., (1977). A histidine-rich protein from Plasmodium falciparum and its interaction with membranes. Bulletin of the World Health Organization 55, 191–7.Google ScholarPubMed
Klei, T. R., & De Giusti, D. L., (1973). Ultrastructural changes in salivary glands of Pseudolynchia canariensis (Diptera: Hippoboscidae) infected with sporozoites of Haemoproteus columbae. Journal of Invertebrate Pathology 22, 321–8.CrossRefGoogle Scholar
Kramptiz, H. E., (1962). Weitere Untersuchungen an Grahamella Brumpt 1911. Zeitschrift für Tropenmedizin und Parasitologie 13, 34–53.Google Scholar
Kramptiz, H. E., & Kleinschmidt, A., (1960). Grahamella Brumpt 1911 biologische und morphologische Untersuchungen. Zeitschrift für Tropenmedizin und Parasitologie 11, 336–52.Google Scholar
Ladda, R. L., Aikawa, M., & Sprinz, H., (1969). Penetration of erythrocytes by merozoites of mammalian and avian malarial parasites. Journal of Parasitology 55, 633–44.CrossRefGoogle ScholarPubMed
Landau, I., Rosin, G., Miltgen, F., Hugot, J.-P., Leger, N., Beveridge, I., & Baccam, D., (1980). Sur le genre Polychromophilus (Haemoproteidae, parasite de Microchiroptères). Annales de Parasitologie Humaine et Comparée 55, 13–32.CrossRefGoogle Scholar
Mer, G. G., & Goldblum, N., (1947). A haemosporidian of bats. Nature, London 159, 444.CrossRefGoogle ScholarPubMed
Molyneux, D. H., & Bafort, J. M., (1971). Observations on the trypanosome of Pipistrellus pipistrellus in Britain, Trypanosoma (Schizotrypanum) vespertilionis. Annales de la Société Beige de Medecin tropicale 51, 335–48.Google Scholar
Schingareff, A. J., (1906). Des hémosporidies des chauves-souris. Archives of Science and Biology of St. Petersburg 12, 182–9.Google Scholar
Sinden, R. E., (1978). Cell biology. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W.), pp. 85–168. London: Academic Press.Google Scholar
Sinden, R. E., (1983). Sexual development of malarial parasites. Advances in Parasitology 22, 153–216.CrossRefGoogle ScholarPubMed
Sinden, R. E., & Garnham, P. C. C., (1973). A comparative study on the ultrastructure of Plasmodium sporozoites within the oocysts and salivary glands, with particular reference to the incidence of the micropore. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 631–7.Google Scholar
Sinden, R. E., Canning, E. U., & Spain, B., (1976). Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: a transmission electron microscope study. Proceedings of the Royal Society of London, B 193, 55–76.Google ScholarPubMed
Sterling, C. R., & Aikawa, M., (1973). A comparative study of gametocyte ultrastructure in avian haemosporidia. Journal of Protozoology 20, 81–92.Google Scholar
Sterling, C. R., Aikawa, M., & Nussenzweig, R. S., (1973). The passage of Plasmodium berghei sporozoites through the salivary glands of Anopheles stephensi: An electron microscope study. Journal of Parasitology 59, 593–605.Google Scholar
Terzakis, J. A., Sprinz, H., & Ward, R. A., (1967). The transformation of the Plasmodium gallinaceum oocyst in Aedes aegypti mosquitoes. Journal of Cell Biology 34, 311–26.Google Scholar
Thompson, G. B., (1972). An annotated bibliography of the British Nycteribiidae. Angewandte Parasitologie 13, 106–13.Google ScholarPubMed
Wong, T. C., & Desser, S. S., (1976). Fine structure of oocyst transformation and the sporozoites of Leucocytozoon dubreuili. Journal of Protozoology 23, 115–26.CrossRefGoogle ScholarPubMed