Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-19T10:17:35.739Z Has data issue: false hasContentIssue false
  • English
  • Français

An evaluation of protozoal characteristics in relation to biological control of pests

Published online by Cambridge University Press:  06 April 2009

Elizabeth U. Canning
Elizabeth U. Canning
Affiliation:
Department of Pure and Applied Biology, Imperial College of Science and Technology, London SW7 2AZ
Get access Rights & Permissions [Opens in a new window]

Summary

Of the unicellular eukaryotes, formerly Protozoa, now considered to belong to five separate phyla, only the neogregarines and microsporidia are serious contenders for a role in biological control of invertebrate pests. Ciliates of the genus Lambornella, which penetrate their hosts via cuticular cysts, have potential in mosquito control but have not been investigated in depth.

‘Protozoa’ generally kill their hosts by overwhelming numbers, destroying the normal function of organs or depleting the host of essential reserves. Because they are slow-acting pathogens they cannot be used on their own when pests have already reached a high level of abundance nor can they be relied upon when the damage threshold of pests is low. Their principal use will be as the slow-acting component of a 2-pathogen or pathogen-plus-chemical formulation, which can be used when a degree of damage is tolerable.

A comparison is made between two microsporidia in lepidopteran hosts, Vairimorpha necatrix and Nosema pyrausta. The former causes high mortality in a wide range of hosts, when bacterial septicaemia ensues after disruption of the gut wall by the microsporidian invasion process. Some larvae may survive this period and live to damage crops, but none survives to adulthood. There is no transovarial transmission and the parasite is rarely found in natural populations. V. necatrix could be used as a microbial pesticide for short-term control. N. pyrausta is restricted to a single host, the European corn borer. It has low pathogenicity, causing some larval mortality especially under conditions of environmental stress. Most hosts survive to adults but show reduced longevity and fecundity. The parasite is transmitted transovarially and is highly prevalent in the field. It is not considered pathogenic enough to be used as a microbial pesticide but is an important factor in regulating natural populations. These examples illustrate the inverse relationship between pathogenicity and prevalence and show how cycles of host population abundance may be driven by pathogens of moderate to low pathogenicity.

Two kinds of transovarial transmission mechanisms are discussed. With the microsporidia of winter moth, vegetative stages and spores, even when abundant in egg yolk, do not gain access to larval tissues but are confined to the meconium in larvae just before eclosion. Larvae are not infected when they hatch but the spores are carried over in the eggs to the next period of larval feeding activity. In contrast, some genera of microsporidia in haematophagous diptera, e.g. Amblysopora in mosquitoes, actually infect the cells of developing larvae, which are already infected when they hatch.

The prospects for biological control with ‘Protozoa’ are reviewed for vectors of medical importance and for pests of pasture, field crops, forests and stored products. Particular attention is given to the use of microsporidia in combination with low concentrations of compatible chemical insecticides and with other pathogens (e.g. viruses).

Spores for field application can be produced in natural or experimental hosts by feeding or intrahaemocoelic inoculation. Yields vary according to the species of parasite and host. Examples are Nosema locustae in Melanoplus bivittatus yielding 3·9 × 109 spores/grasshopper enough to treat more than 1 hectare of rangeland, and Vairimorpha necatrix in Heliothis zea, yielding 1·67 × 109 spores per larva, with 2·5 × 1012 spores/hectare required for field application. In vitro culture is at present a laboratory tool only, with yields too low for economic returns.

Spores can be stored, according to species, dry or in distilled water with antibiotics at 4 °C. This gives good survival for months or years. In field applications feeding-bait formulations are more efficacious than sprays because they concentrate the spores for uptake by the target species and give the spores some protection from harmful ultraviolet radiation.

Pheromone lures have been used for the introduction of spores by males into pest infestations in stored grain. Males are lured to sites dusted with spores and return to the grain after removal of the lure, to contaminate females and larvae. The use of these lures, first as traps to monitor pest population increases, then to effect a controlled pest growth curve by introduction of pathogens, is an attractive innovation. Protozoa are considered safe for field application on the limited evidence available.

Type
Research Article
Information
Parasitology , Volume 84 , Issue 4 , April 1982 , pp. 119 - 149
Copyright
Copyright © Cambridge University Press 1982

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

Ahamed, A. & Narasimhamurti, C. C. (1977). A new species of Malamoeba, M. indica n.sp. from the Malpighian tubules of the painted grasshopper Poecilocerca picta Fabr. 5th International Congress of Protozoology,New York. Abstract.Google Scholar
Alger, N. E. & Undeen, A. H. (1970). The control of a microsporidian Nosema sp., in an anopheline colony by an egg-rinsing technique. Journal of Invertebrate Pathology 15, 321–7.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1980). Infectious diseases and population cycles of forest insects. Science 210, 658–61.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1981). The population dynamics of microparasites within invertebrate populations. Philosophical Transactions of the Royal Society, B 291, 451–524.Google Scholar
Andreadis, T. G. & Hall, D. W. (1979). Development, ultrastructure, and mode of transmission of Amblyospora sp. (Microspora) in the mosquito. Journal of Protozoology 26, 444–52.CrossRefGoogle ScholarPubMed
Antony, D. W., Savage, K. E., Hazard, E. I., Avery, S. W., Boston, M. D. & Oldacre, S. W. (1978). Field tests with Nosema algerae Vávra and Undeen (Microsporida, Nosematidae) against Anopheles albimanus Wiedemann in Panama. Miscellaneous Publications of the Entomological Society of America 11, 17–27.Google Scholar
Antony, D. W., Savage, K. E. & Weidhaas, D. E. (1972). Nosematosis: its effect on Anopheles albimanus Wiedemann, and a population model of its relation to malaria transmission. Proceedings of the Helminthological Society of Washington, 39, 428–33.Google Scholar
Bailey, L. (1972). The preservation of infective microsporidian spores. Journal of Invertebrate Pathology 20, 252–4.CrossRefGoogle Scholar
Bano, L. (1958). Partial inhibitory effect of Plistophora culicis on the sporogonic cycle of Plasmodium cynomolgi in Anopheles stephensi. Nature, London 181, 430.CrossRefGoogle ScholarPubMed
Barker, R. J., Smith, J. & Lai, P. F. (1980). The culture of the microsporidian parasites Nosema algerae and N. eurytremae in vertebrate cells. Journal of Protozoology 27, 55A.Google Scholar
Bayne, C. J., Owczarzak, A. & Noonan, W. E. (1975). In vitro cultivation of cells and a microsporidian parasite of Biomphalaria glabrata (Pulmonata, Basommatophora). Annals of the New York Academy of Science 266, 513–27.CrossRefGoogle Scholar
Brooks, W. M. (1968). Transovarian transmission of Nosema heliothidis in the corn earworm Heliothis zea. Journal of Invertebrate Pathology 11, 511–12.CrossRefGoogle Scholar
Brooks, W. M. (1980). Production and efficacy of Protozoa. Biotechnology and Bioengineering 22, 1415–40.CrossRefGoogle Scholar
Burkholder, W. E. (1981). Biomonitoring for stored-product insects. In Management of Insect Pests with Semiochemicals (ed. Mitchell, E. R.), pp. 29–40. Plenum Publishing Corporation.CrossRefGoogle Scholar
Burkholder, W. E. (1981). Biological suppression of stored-product insect pests. 5th Beltsville Agricultural Research Center Symposium (ed.Papavisas, G.) (in the Press). New Jersey: Allanheld Osmun & Co.Google Scholar
Canning, E. U. (1975). The microsporidian parasites of Platyhelminthes: their morphology, development, transmission and pathogenicity. Commonwealth Institute of Helminthology, Miscellaneous Publications No. 2, pp. 1–32.Google Scholar
Canning, E. U. (1981). Insect control with Protozoa. In Biological Control in Crop Production, 5th Beltsville Agricultural Research Center Symposium (ed. Papavisas, G.), (in the Press). New Jersey: Allanheld Osmun & Co.Google Scholar
Canning, E. U. & Barker, R. J. (1981). Transmission of microsporidia between generations of winter moth Operophtera brumata. Parasitology (in the Press).Google Scholar
Canning, E. U. & Basch, P. (1968).Perezia helminthorum sp.nov., amicrosporidian hyperparasite of trematode larvae from Malaysian snails. Parasitology 58, 341–7.CrossRefGoogle Scholar
Canning, E. U., Higby, G. C. & Nicholas, J. P. (1979). An experimental study of the effects of Nosema eurytremae (Microsporida: Nosematidae) on the liver fluke Fasciola hepatica. Parasitology 79, 381–92.CrossRefGoogle ScholarPubMed
Canning, E. U. & Hulls, R. H. (1970). A microsporidian infection of Anopheles gambiae Giles, from Tanzania, interpretation of its mode of transmission and notes on Nosema infections in mosquitoes. Journal of Protozoology 17, 531–9.CrossRefGoogle Scholar
Clark, T. B. & Brandl, D. G. (1976). Observations on the infection of Aedes sierrensis by a tetrahymenine ciliate. Journal of Invertebrate Pathology 28, 341–9.CrossRefGoogle ScholarPubMed
Corbel, J. C. (1967). Les parasites des Orthoptères. Année Biologique 6, 391–428.Google Scholar
Corliss, J. O. & Coats, D. W. (1976). A new cuticular cyst-producing tetrahymenid ciliate, Lambornella clarki n.sp. and the current status of ciliatosis in culicine mosquitoes. Transactions of the American Microscopical Society 95, 725–39.CrossRefGoogle Scholar
Costa, C. A. F. & Bradley, R. E. (1980). Hyperparasitism of intrasnail stages of Fasciola hepatica by a mosquito microsporidian parasite. Journal of Invertebrate Pathology 35, 175–81.CrossRefGoogle ScholarPubMed
Davies, K. A. (1973). Observations on Malamoeba locustae from Chorloicetes terminifera cultures in Australia. Journal of Invertebrate Pathology 22, 475.CrossRefGoogle Scholar
Evans, W. A. & Elias, R. G. (1970). The life cycle of Malamoeba locustae (King et Taylor) in Locusta migratoria (R. & F.). Acta Protozoologica 7, 229–41.Google Scholar
Fine, P. E. M. (1981). Vertical transmission of pathogens of invertebrates. In Comparative Pathobiology, vol. 6 (ed. Bulla, L. A. and Cheng, T. C.) (in the Press). New York: Plenum Press.Google Scholar
Franz, J. M. & Huger, A. M. (1971). Microsporidia causing the collapse of an outbreak of the green tortrix (Tortrix viridana L.) in Germany. Proceedings of the 4th International Colloquium on Insect Pathology,College Park, Maryland, pp. 48–53.Google Scholar
Fuxa, J. R. & Brooks, W. M. (1978). Persistence of spores of Vairimorpha necatrix on tobacco, cotton, and soybean foliage. Journal of Economic Entomology 71, 169–72.CrossRefGoogle Scholar
Fuxa, J. R. & Brooks, W. M. (1979 a). Mass production and storage of Vairimorpha necatrix (Protozoa: Microsporida). Journal of Invertebrate Pathology 33, 86–94.CrossRefGoogle Scholar
Fuxa, J. R. & Brooks, W. M. (1979 b). Effects of Vairimorpha necatrix in sprays and corn meal on Heliothis species in tobacco, soybeans and sorghum. Journal of Economic Entomology 72, 462–7.CrossRefGoogle Scholar
Gaugler, R. R. & Brooks, W. M. (1975). Sublethal effects of infection by Nosema heliothidis in the corn earworm, Heliothis zea. Journal of Invertebrate Pathology 26, 57–63.CrossRefGoogle Scholar
Gupta, K. S. (1964). Cultivation of Nosema mesnili Paillot (Microsporidia) in vitro. Current Science, India 33, 407–8.Google Scholar
Hanrahan, S. A. (1979). Malamoeba locustae its ultrastructure and its influence on the locust host. Ph.D. thesis, University of the Witwatersrand, Johannesburg, pp. 284.Google Scholar
Hazard, E. I. (1970). Microsporidian diseases in mosquito colonies: Nosema in two Anopheles colonies. Proceedings of the 4th International Colloquium on Insect Pathology,College Park, Maryland, pp. 267–71.Google Scholar
Hazard, E. I., Andreadis, T. G., Joslyn, D. J. & Ellis, E. A. (1979). Meiosis and its implications in the life cycles of Amblyospora and Parathelohania (Microspore). Journal of Parasitology 65, 117–22.CrossRefGoogle Scholar
Hazard, E. I. & Lofgren, C. S. (1971). Tissue specificity and systematics of a Nosema in some species of Aedes, Anopheles and Culex. Journal of Invertebrate Pathology 18, 16–24.CrossRefGoogle ScholarPubMed
Hazard, E. I. & Oldacre, S. W.. (1976). Revision of Microsporidia (Protozoa) close to Thelohania with descriptions of one new family, eight new genera and thirteen new species. United States Department of Agriculture Technical Bulletin No. 1530, pp. 1–104.Google Scholar
Henry, J. E. (1981). Natural and applied control of insects by Protozoa. Annual Reviews of Entomology 26, 49–73.CrossRefGoogle Scholar
Henry, J. E. & Oma, E. A. (1981). Protozoa: pest control by Nosema locustae, a pathogen of grasshoppers and crickets. In Microbial Control of Pests and Plant Diseases, 1976–1980 (ed.Burges, H. D.), pp. 573–86. New York and London: Academic Press.Google Scholar
Higby, G. C., Canning, E. U., Pilley, B. M. & Bush, P. J. (1979). Propagation of Nosema eurytremae (Microsporidia: Nosematidae) from trematode, larvae in abnormal hosts and in tissue culture. Parasitology 78, 155–70.CrossRefGoogle Scholar
Hill, R. E. & Gary, W. J. (1979). Effects of the microsporidium, Nosema pyrausta, on field populations of European corn borers in Nebraska. Environmental Entomology 8, 91–5.CrossRefGoogle Scholar
Hulls, R. H. (1972). Studies on microsporidia of mosquitoes and their relationship with Plasmodium berghei. Ph.D. thesis, University of London, pp. 199.Google Scholar
Ignoffo, C. M. & Hink, W. F. (1971). Propagation of arthropod pathogens in living systems. In Microbial Control of Insects and Mites (ed. Burges, H. D. and Hussey, N. W.), pp. 541–80. New York and London: Academic Press.Google Scholar
Ignoffo, C. M., Hostetter, D. L., Sikorowski, P. P., Sutter, G. & Brooks, W. M. (1977). Inactivation of representative species of entomopathogenic viruses, a bacterium, fungus and protozoan by an ultraviolet light source. Environmental Entomology 6, 411–15.CrossRefGoogle Scholar
Ishihara, R. (1969). The life cycle of Nosema bombycis as revealed in tissue culture cells of Bombyx mori. Journal of Invertebrate Pathology 14, 316–20.CrossRefGoogle ScholarPubMed
Ishihara, R. & Sohi, S. S. (1966). Infection of ovarian tissue cultures of Bombyx mori by Nosema bombycis spores. Journal of Invertebrate Pathology 8, 538–40.CrossRefGoogle Scholar
Kaya, H. K. (1973). Pathogenicity of Pleistophora schubergi to larvae of the orange-striped oakworm and other lepidopterous insects. Journal of Invertebrate Pathology 22, 356–8.CrossRefGoogle Scholar
Kaya, H. K. (1975). Persistence of spores of Pleistophora schubergi (Cnidospora, Microsporidia) in the field, and their application in microbial control. Journal of Invertebrate Pathology 26, 329–32.CrossRefGoogle Scholar
Kaya, H. K. (1977). Survival of spores of Vairimorpha (= Nosema) necatrix (Microsporidia: Nosematidae) exposed to sunlight, ultra-violet radiation and high temperature. Journal of Invertebrate Pathology 30, 192–8.CrossRefGoogle Scholar
King, R. L. & Taylor, A. B. (1936). Malpigamoeba locustae, n.sp. (Amoebidae), a protozoan parasitic in the Malpighian tubes of grasshoppers. Transactions of the American Microscopical Society 55, 6–10.CrossRefGoogle Scholar
Kramer, J. P. (1959 a). Some relationships between Perezia pyraustae Paillot (Sporozoa, Nosematidae) and Pyrausta nubilalis (Hübner) (Lepidoptera, Pyralidae). Journal of Insect Pathology 1, 25–33.Google Scholar
Kramer, J. P. (1959 b). Observations on the seasonal incidence of microsporidiosis in European corn borer populations in Illinois. Entomophaga 4, 37–42.CrossRefGoogle Scholar
Kramer, J. P. (1970). Longevity of microsporidian spores with special reference to Octosporea muscaedomesticae Flu. Acta Protozoologica 8, 217–24.Google Scholar
Kramer, J. P. (1976). The extra-corporeal ecology of microsporidia. In Comparative Pathobiology, vol. 1. Biology of the Microsporidia (ed. Bulla, L. A. and Cheng, T. C.), pp. 127–135.Google Scholar
Kurtti, T. J. & Brooks, M. A. (1971). Growth of a microsporidian parasite in cultured cells of tent caterpillars (Malacosoma). Current Topics in Microbiology and Immunology 55, 204–8.Google ScholarPubMed
Kurtti, T. J. & Brooks, M. A. (1977). The rate of development of a microsporidian in moth cell culture. Journal of Invertebrate Pathology 29, 126–32.CrossRefGoogle Scholar
Lai, P. F. (1980). Microsporidia in Schistosoma mansoni and their propagation in vivo and in vitro. Ph.D. thesis, University of London, p. 252.Google Scholar
Lai, P. F. & Canning, E. U. (1980). Infectivity of a microsporidium of mosquitoes (Nosema algerae) to larval stages of Schistosoma mansoni in Biomphalaria glabrata. International Journal of Parasitology 10, 293–301.CrossRefGoogle ScholarPubMed
Lai, P. F. & Canning, E. U. (1981). Some factors affecting spore replication of Nosema algerae (Microspore, Nosematidae) in Pieris brassicae (Lepidoptera). Journal of Invertebrate Pathology (in the Press).Google Scholar
Larsson, R. (1976). Insect pathological investigations on Swedish Thysanura. 1. Observations on Malamoeba locustae (Protozoa, Amoebidae) from Lepisma saccharina (Thysanura, Lepismatidae). Journal of Invertebrate Pathology 28, 43–6.CrossRefGoogle Scholar
Lea, A. (1958). Recent outbreaks of the brown locust, Locustana pardalina (Walk.) with special references to the influence of rainfall. Journal of the Entomological Society of South Africa 21, 18–35.Google Scholar
Levine, N. D., Corliss, J. O., Cox, F. E. G., Deroux, G., Grain, J., Honigberg, B. M., Leedale, G. F., Loeblich, A. R. III, Lom, J., Lynn, D., Merinfield, E. G., Page, F. C., Poijansky, G., Sprague, V., Vávra, J. & Wallace, F. G. (1980). A newly revised classification of the Protozoa. Journal of Protozoology 27, 37–58.CrossRefGoogle ScholarPubMed
Lipa, J. J. & Madziara-Borusiewicz, K. (1976). Microsporidians parasitizing the green tortrix (Tortrix viridana L.) in Poland and their role in the collapse of the tortrix outbreak in Puszcza Niepolomicka during 1970–1974. Acta Protozoologica, Warsaw 15, 529–36.Google Scholar
Loubès, C. (1979). Recherches sur la meiose chez les microsporidies: conséquences sur les cycles biologiques. Journal of Protozoology 26, 200–8.CrossRefGoogle Scholar
Lublinkhof, J., Lewis, L. C. & Berry, E. C. (1979). Effectiveness of integrating insecticides with Nosema pyrausta for suppressing populations of the European corn borer. Journal of Economic Entomology 72, 880–3.CrossRefGoogle Scholar
Maddox, J. V. (1973). The persistence of the microsporidia in the environment. Miscellaneous Publications of the Entomological Society of America 9, 99–104.Google Scholar
Maddox, J. V. (1977). Stability of entomopathogenic Protozoa. Miscellaneous Publications of the Entomological Society of America 10, 3–18.Google Scholar
Maddox, J. V., Brooks, W. M. & Fuxa, J. R. (1981). Vairimorpha necatrix a pathogen of agricultural pests: potential for pest control. In Microbial Control of Pests and Plant Diseases 1976–1980 (ed. Burges, H. D.), pp. 587–94. New York and London: Academic Press.Google Scholar
Mabgileth, A. M., Strano, A. J., Chandra, R., Neafie, R., Blum, M. & McCully, R. M. (1973). Disseminated nosematosis in an immunologically compromised infant. Archives of Pathology 95, 145–50.Google Scholar
Maurand, J. (1973). Recherches biologiques sur les microsporidies des larves de simulies. Dr Sciences thesis, University of Montpellier, p. 199.Google Scholar
McLaughlin, R. E. (1966). Infection of the boll weevil with Mattesia grandis induced by a feeding stimulant. Journal of Economic Entomology 59, 909–11.CrossRefGoogle Scholar
McLaughlin, R. E. (1967). Development of the bait principle for boll-weevil control. II. Field-cage tests with a feeding stimulant and the protozoan Mattesia grandis. Journal of Invertebrate Pathology 9, 70–7.CrossRefGoogle Scholar
McLaughlin, R. E. (1971). Use of protozoans for microbial control of insects. In Microbial Control of Insects and Mites (ed. Burges, H. D. and Hussey, N. W.), pp. 151–72. New York and London: Academic Press.Google Scholar
McLaughlin, R. E. & Bell, M. R. (1970). Mass production in vivo of two protozoan pathogens, Mattesia grandis and Glugea gasti of the boll weevil, Anthonomis grandis. Journal of Invertebrate Pathology 16, 84–8.CrossRefGoogle Scholar
McLaughlin, R. E., Cleveland, T. C., Daum, R. J. & Bell, M. R. (1969). Development of the bait principle for boll-weevil control. IV. Field tests with a bait containing a feeding stimulant and the sporozoans Glugea gasti and Mattesia grandis. Journal of Invertebrate Pathology 13, 429–41.CrossRefGoogle Scholar
McLaughlin, R. E., Daum, R. J. & Bell, M. R. (1968). Development of the bait principle for boll-weevil control. III. Field-cage tests with a feeding stimulant and the protozoans Mattesia grandis (Neogregarinida) and a microsporidian. Journal of Invertebrate Pathology 12, 168–74.CrossRefGoogle Scholar
Michaelson, E. H. (1963). Plistophora husseyi sp.n., a microsporidian parasite of aquatic pulmonate snails. Journal of Insect Pathology 5, 28–38.Google Scholar
Milner, R. J. (1972). The survival of Nosema whitei spores stored at 4 °C. Journal of Invertebrate Pathology 20, 256–7.CrossRefGoogle Scholar
Mistric, W. J. & Smith, F. D. (1973). Tobacco budworm: control on flue-cured tobacco with certain microbial pesticides. Journal of Economic Entomology 66, 979–82.CrossRefGoogle Scholar
Nordin, G. L. & Maddox, J. V. (1972). Effects of simultaneous virus and microsporidian infections on larvae of Hyphantria cunea. Journal of Invertebrate Pathology 20, 66–9.CrossRefGoogle Scholar
Oshima, K. (1964). Method of gathering and purifying active spores of Nosema bombycis and preserving them in good condition. Annotationes Zoologicae Japonenses 37, 94–101.Google Scholar
Pilley, B. M., Barker, R. J., Canning, E. U. & Hammond, J. C. (1978). Bioassay of Nosema eurytremae (Protozoa, Microsporida) hyperinfecting Schistosoma mansoni in Biomphalaria glabrata. Proceedings of the 2nd International Colloquium on Invertebrate Pathology,Prague, pp. 151–2.Google Scholar
Pilley, B. M., Canning, E. U. & Hammond, J. C. (1978). The use of a micro-injection procedure for large scale production of the microsporidian Nosema eurytremae. Journal of Invertebrate Pathology 32, 355–8.CrossRefGoogle Scholar
Prinsloo, H. E. (1960). Parasitiese mikro-organismes by die bruinsprinkaan Locustana pardalina (Walk). South African Journal of Agricultural Science 3, 551–60.Google Scholar
Reynolds, D. G. (1970). Laboratory studies of the microsporidian Plistophora culicis (Weiser) infecting Culex pipiens fatigans Wied. Bulletin of Entomological Research 60, 339–49.CrossRefGoogle ScholarPubMed
Reynolds, D. G. (1972). Experimental introduction of a microsporidian into a wild population of Culex pipiens fatigans Wied. Bulletin of the World Health Organization 46, 807–12.Google ScholarPubMed
Savage, K. E. & Lowe, R. E. (1970). Studies on Anopheles quadrimaculatus infected with a Nosema sp. Proceedings of the 4th International Colloquium on Insect Pathology,College Park, Maryland, pp. 272–8.Google Scholar
Savage, K. E., Lowe, R. E., Hazard, E. I. & Lofgren, C. S. (1972). Studies on the transmission of Plasmodium gallinaceum by Anopheles quadrimaculatus infected with a Nosema sp. Bulletin of the World Health Organization 45, 845–7.Google Scholar
Schwalbe, C. P., Burkholder, W. E. & Boush, G. M. (1974). Mattesia trogodermae infection rates as influenced by mode of transmission, dosage and host species. Journal of Stored Products Research 10, 161–6.CrossRefGoogle Scholar
Seibold, H. R. & Fussell, E. N. (1973). Intestinal microsporidiosis in Callicebus moloch. Laboratory Animal Science 23, 115–18.Google ScholarPubMed
Shapas, T. J., Burkholder, W. E. & Boush, G. M. (1977). Population suppression of Trogoderma glabrum by using pheromone luring for protozoan pathogen dissemination. Journal of Economic Entomology 70, 469–74.CrossRefGoogle Scholar
Sikorowski, P. P. & Lashomb, J. H. (1977). Effect of sunlight on the infectivity of Nosema heliothidis spores isolated from Heliothis zea. Journal of Invertebrate Pathology 30, 95–6.CrossRefGoogle ScholarPubMed
Sneller, V.-P. (1979). Inhibition of Dirofilaria immitis in gregarine-infected Aedes aegypti: preliminary observations. Journal of Invertebrate Pathology 34, 62–70.CrossRefGoogle ScholarPubMed
Sohi, S. S. & Wilson, G. G. (1976). Persistent infection of Malacosoma disstria (Lepidoptera, Lasiocampidae) cell cultures with Nosema (Glugea) disstriae (Microsporidia: Nosematidae). Canadian Journal of Zoology 54, 336–42.CrossRefGoogle Scholar
Steinhaus, E. A. (1951). Report on diagnoses of diseased insects 1944–50. Hilgardia 20, 629–78.CrossRefGoogle Scholar
Streett, D. A., Ralph, D. & Hink, W. F. (1980). Replication of Nosema algerae in three insect cell lines. Journal of Protozoology 27, 113–17.CrossRefGoogle Scholar
Tanada, Y. (1964). Incidence of microsporidiosis in field population of the armyworm, Pseudaletia unipuncta (Haworth). Proceedings of the Hawaiian Entomological Society 3, 435–6.Google Scholar
Tanada, Y. & Chang, G. Y. (1962). An epizootic resulting from a microsporidian and two virus infections in the army-worm, Pseudaletia unipuncta (Haworth). Journal of Insect Pathology 4, 129–31.Google Scholar
Taylor, A. B. & King, R. L. (1937). Further studies on the parasitic amebae found in grasshoppers. Transactions of the American Microscopical Society 56, 172–6.CrossRefGoogle Scholar
Teetor, G. E. & Kramer, J. P. (1977). Effect of ultraviolet radiation on the microsporidian Octosporea muscaedomesticae with reference to protectants provided by the host Phormia regina. Journal of Invertebrate Pathology 30, 348–53.CrossRefGoogle ScholarPubMed
Thomson, H. W. (1958). The effect of a microsporidian parasite on the development, reproduction and mortality of the spruce budworm, Choristoneura fumiferana (Clem). Canadian Journal of Zoology 36, 499–511.CrossRefGoogle Scholar
Undeen, A. H. (1975). Growth of Nosema algerae in pig kidney cell cultures. Journal of Protozoology 22, 107–10.CrossRefGoogle ScholarPubMed
Undeen, A. H. & Alger, N. (1976). Nosema algerae: infection of the white mouse by a mosquito parasite. Experimental Parasitology 40, 86–8.CrossRefGoogle ScholarPubMed
Undeen, A. H. & Maddox, J. V. (1973). The infection of non-mosquito hosts by injection with spores of the microsporidian Nosema algerae. Journal of Invertebrate Pathology 22, 258–65.CrossRefGoogle Scholar
Van Denburgh, R. S. & Burbutis, P. B. (1962). The host parasite relationship of the European corn borer, Ostrinia nubilalis, on the protozoan, Perezia pyraustae, in. Delaware. Journal of Economic Entomology 55, 65–7.CrossRefGoogle Scholar
Vávra, J., Canning, E. U., Barker, R. J. & Desportes, I. (1981). Characters of microsporidian genera (Workshop Proceedings, EMOP 3). Parasitology 82, 131–42.Google Scholar
Vávra, J. & Maddox, J. V. (1976). Methods in microsporidiology. In Comparative Pathobiology, vol. 1, Biology of the Microsporidia (ed. Bulla, L. A. and Cheng, T. C.), pp. 281–319.Google Scholar
Vávra, J. & Undeen, A. H. (1970). Nosema algerae n.sp. (Cnidospora: Microsporidia) a pathogen in a laboratory colony of Anopheles stephensi Liston (Diptera: Culicidae). Journal of Protozoology 17, 240–9.CrossRefGoogle Scholar
Vávra, J. & Undeen, A. H. (1981). Microsporidia (Microspore: Microsporida) from Newfoundland blackflies (Diptera: Simuliidae). Canadian Journal of Zoology 59, 1431–46.CrossRefGoogle Scholar
Venter, I. G. (1966). Egg development in the brown locust, Locustana pardalina (Walker) with special reference to the effect of infestation by Malamoeba locustae. South African Journal of Agricultural Science 9, 429–34.Google Scholar
Wallace, F. G. (1979). Biology of the Kinetoplastida of arthropods. In Biology of the Kinetoplastida, vol. 2 (ed. Lumsden, W. H. R. and Evans, D. A.), pp. 213–40.Google Scholar
Weiser, J. & Veber, J. (1954). Možnosti biologickeho boje s prastevnickem americkým (Hyphantria cunea Drury). II. Československá Parasitologic Praha 2, 191–9.Google Scholar
Weiser, J. & Veber, J. (1957). Die Mikrosporidie Thelohania hyphantriae Weiser des weissen Bärenspinners und anderer Mitglieder seiner Biocönose. Zeitschrift für angewandle Entomologie 40, 55–70.CrossRefGoogle Scholar
Wilson, G. G. (1974). The effects of temperature and ultraviolet radiation on the infection of Choristoneura fumiferana and Malacosoma pluviale by a microsporidian parasite Nosema (Perezia) fumiferanae (Thom.). Canadian Journal of Zoology 52, 59–63.CrossRefGoogle Scholar
Wilson, G. G. (1978). Microsporidian infection in spruce budworm (Choristoneura fumiferana) 1 and 2 years after application. Bi-monthly Research Notes of the Canadian Foresty Service 34, 16.Google Scholar
Wilson, G. G. & Kaupp, W. J. (1975). Application of a microsporidia Nosema fumiferanae against spruce budworm on Manitoulin Island, 1975. Environment of Canada Information Report No. IP-X-11, p. 26.Google Scholar
Wilson, G. G. & Kaupp, W. J. (1976 a). A preliminary field trial using Nosema fumiferanae against the spruce budworm, Choristoneura fumiferana. Bi-monthly Research Notes of the Canadian Forestry Service 32, 2–3.Google Scholar
Wilson, G. G. & Kaupp, W. J. (1976 b). Application of Nosema fumiferanae and Pleistophora schubergi against spruce budworm in Ontario, 1976. Environment of Canada Information Report no. IP-X-15, p. 15.Google Scholar
Wilson, G. G. & Kaupp, W. J. (1977). Application of Nosema disstriae and Pleistophora schubergi against forest tent caterpillar in Ontario, 1977. Report of the Forest Pest Management Institute Sault Sainte Marie No. FMP-X-4, p. 9.Google Scholar
Zimmack, H. L., Arbuthnot, K. D. & Brindley, T. A. (1954). Distribution of the European corn borer parasite Perezia pyraustae and its effect on the host. Journal of Economic Entomology 47, 641–5.CrossRefGoogle Scholar
Zimmack, H. L. & Brindley, T. A. (1957). The effect of the protozoan parasite Perezia pyraustae Paillot on the European corn borer. Journal of Economic Entomology 50, 637–40.CrossRefGoogle Scholar