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Host reactions of Musca domestica, Orthellia caesarion, and Ravinia I'herminieri to the nematode Heterotylenchus autumnalis*

Published online by Cambridge University Press:  06 April 2009

John G. Stoffolano Jr.  and
Frederick A. Streams
John G. Stoffolano Jr.
Affiliation:
Biological Sciences Group, Ecology Section, University of Connecticut, Storrs, Connecticut 06268
Frederick A. Streams
Affiliation:
Biological Sciences Group, Ecology Section, University of Connecticut, Storrs, Connecticut 06268
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Summary

The nematode, Heterotylenehus autumnalis, generally failed to develop successfully in Musca domestica L., Orthellia caesarion (Meigen) and Ravinia l'herminieri(Robineau-Desvoidy). Failure is attributed mainly to host resistance in the form of haemocytic encapsulation of the small gamogenetic female nematode. In a few instances, the nematode was able to complete development successfully in housefly and Orthellia, but was not capable of leaving the host. These few instances of development in the unnatural, experimental hosts are attributed in part to general ’weakening’ of the host by superparasitism. In many cases superparasitism resulted in the death of the fly larvae or pupae.

Tracheolar proliferation was usually associated with the encapsulated nematodes and there was evidence that many of them were expelled from the host during pupation. We also observed nematodes with cephalic caps of dark material, presumably melanin, and some that were tightly girdled with this material. A host reaction, apparently never before reported for a parasitized insect, was the darkening (presumably melanization) of the larval anal organ.

The authors would like to express their appreciation to Dr A. J. Nappi, Biology Department, State University of New York, Oswego, New York, and Dr G. 0. Poinar, Jr., Department of Entomology and Parasitology, University of California, Berkeley, California, for reading an early draft of the manuscript and offering critical comments. The senior author would like to express his deep appreciation to Dr W. R. Nickle, Nematology Investigations, Crops Research Division, Agr. Res. Serv., USDA, Beltsville, Maryland, and to Dr H. Welch, Zoology Department, University of Manitoba, Winnipeg, Canada, for their help and encouragement during the course of this study. This study was supported in part by a grant from the University of Connecticut Research Foundation.

Type
Research Article
Information
Parasitology , Volume 63 , Issue 2 , October 1971 , pp. 195 - 211
Copyright
Copyright © Cambridge University Press 1971

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References

REFERENCES

Alicata, J. E. (1935). Early developmental stages of nematodes occurring in swine. Technical Bulletin No. 489, pp. 1–96. Washington, D.C.: United States Department of Agriculture.Google Scholar
Blume, R. R. (1970). Insects associated with bovine droppings in Kerr and Bexar Counties, Texas. Journal of Economic Entomology 63, 1023–4.CrossRefGoogle Scholar
Bovien, P. (1937). Some types of association between nematodes and insects. Vidensakabelige Meddelelser fra Dansk naturhistorisk Forening i Kjøbenhaven 101, 1–114.Google Scholar
Bovien, P. (1944). Proactractonema sciarae n.g., n.sp., a parasitic nematode from the body cavity of a dipterous larva. Videnskabelige Meddelelser fra Dansk naturhistorisk Forening i Kjøbenhavn 108, 1–14.Google Scholar
Bronskill, J. F. (1962). Encapsulation of rhabditoid nematodes in mosquitoes. Canadian Journal of Zoology 40, 1269–75.CrossRefGoogle Scholar
Brug, S. L. (1932). Chitinization of parasites in mosquitoes. Bulletin of Entomological Research 23, 229–31.CrossRefGoogle Scholar
Burns, W. C. (1961). Penetration and development of Allassogonoporus vespertilions and Acanthatrium oregonense (Trematoda: Lecithodendriidae) cercariae in caddis fly larvae. Journal of Parasitology 47, 927–32.CrossRefGoogle ScholarPubMed
Chen, H. T. (1933). On a method of expelling disintegrated tapeworms in Ctenocephalides felis. Lingnan Science Journal, Supplementyes 12, 43–48.Google Scholar
Desowitz, R. S. & Challappah, W. T. (1965). Fate of transplanted third-stage Brugia pahangi larvae in normally susceptible and non-susceptible hosts. Journal of Parasitology 51, 195–9.CrossRefGoogle Scholar
Doutt, R. L. (1963). Pathologies caused by insect parasites. In Insect Pathology, an advanced treatise, Vol. 2, pp. 393–422. Ed. Steinhaus, E. A.. New York: Academic Press.CrossRefGoogle Scholar
Esslinger, J. H. (1962). Behaviour of microfllariae of Brugia pahangi in Anopheles quadrimaculatus. American Journal of Tropical Medicine 11, 749–58.Google Scholar
Foster, A. O. & Johnson, C. M. (1939). A preliminary note on the identity, life-cycle and pathogenicity of an important nematode parasite of captive monkeys. American Journal of Tropical Medicine 19, 265–72.Google Scholar
Fuchs, G. (1915). Die Naturgeschichte der Nematoden und einiger anderer Parasiten. 1 Des Ips typographus L. 2. Des Hylobius abietis L. Zoologische Jahrbucher (A) Abt. Fur Systematik, Oekologie und Geographie der Tiere 38, 109–22.Google Scholar
Fülleporn, F.(1929). Filariosen des Menschen. In Hanbuch der Pathogenen Mikroorganismen, Bd. 6, pp. 1043–224, 3rd edition. Ed. Kolle, W., Kraus, R. und Uhlenhuth, P.Jena: Gustav Fischer.Google Scholar
Hattingen, R. (1956). Beitrate zur Biologie von Sphaerularia bombi Leon Dufour (1837). Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene, Abt. 2 109, 236–49.Google Scholar
Highby, P. R. (1943). Mosquito vectors and larval development of Dipetalonema arbuta Highby (Nematoda) from the porcupine, Erethizon dorsatum. Journal of Parasitology 29, 243–52.CrossRefGoogle Scholar
Houser, E. C. & Wingo, C. W. (1967). Laboratory culture and biology of Orthellia caesarion with notes on determining larval instars. Journal of Economic Entomology 60, 1355–58.CrossRefGoogle Scholar
Hoy, J. M. (1954). The biology and host range of Neoaplectana leucaniae, a new species of insect-parasitic nematode. Parasitology 44, 393–9.CrossRefGoogle ScholarPubMed
Hu, S. M. K. (1939). Observations of the development of ifiarial larvae during the winter season in Shanghai region. American Journal of Hygiene 29, 67–74.Google Scholar
Hughes, R. D. & Nicholas, W. L. (1969). Heterotylenchus spp. parasitizing the Australian Bush Fly: additional information on the origin of the parasite of the face fly. Journal of Economic Entomology 62, 520–1.CrossRefGoogle Scholar
Jones, C. M. & Perdue, J. M. (1967). Heterotylenchus autumnalis, a parasite of the face fly. Journal of Economic Entomology 60, 1393–5.CrossRefGoogle Scholar
Kartman, L. (1957). The vector of canine filariasis: a review with special reference to factors influencing susceptibility. Revista brasileira de malariologia e doengas tropicais 5, 1–44.Google Scholar
Keilin, D. & Robinson, V. C. (1933). The morphology and life history of Aproctonema entomophagum Keilin, a nematode parasite in the larva of Sciara pullula Winn (Diptera, Nematocera). Parasitology 25, 285–95.CrossRefGoogle Scholar
Kilby, B. A. (1963). The biochemistry of the insect fat body. In Advances in Insect Physiology, Vol. 1, 111–74. Ed. Treherne, J. E. and Wigglesworth, V. B.New York: Academic Press.Google Scholar
Kloft, W. (1949). Über de Einfluss von Mermisparasitismus auf den Stoffwechsel und die Organbildung bei Ameisen. Zeitschrift fur Parasitenkunde 14, 390–422.CrossRefGoogle Scholar
Kurochkin, Y. V. (1961). The nematode Heterotylenchus pawlowskyi n.sp. castrating flea carriers of plague (in English). Doklady Akademii Nauk SSSR — Doklady Biological Sciences Sections — Translation 135, 952–4.Google Scholar
Lavoipierre, M. M. J. (1958). Studies on the host—parasite relationships of filarial nematodes and their arthropod hosts. I. The sites of development and the migration of Loa loa in Chrysops silacea, the escape of the infective forms from the head of the fly, and the effect of the worm on its insect host. Annals of Tropical Medicine and Parasitology 52, 103–21.CrossRefGoogle Scholar
Manson-Bahr, P. H. (1921). Manson's Tropical Diseases, 7th ed. London: Cassell.Google Scholar
Nappi, A.J. (1970). Defense reactions of Drosophila euronotus larvae against the hymonopterous parasite Pseudeucoila bochei. Journal of Invertebrate Pathology. 16, 408–18.CrossRefGoogle ScholarPubMed
Nappi, A. J. & Stoffolano, J. G. Jr. (1971). Heterotylenchus autumnalis: hemocytic reactions and capsule formation in the host, Musca domestica. Experimental Parasitology 29, 116–25.CrossRefGoogle Scholar
Palm, N. B. (1948). Normal and pathological histology of the ovaries in Bombus Latr. with notes on the hormonal inter-relations between the ovaries and the corpora allata. Opuscula entomologica, Supplementyes 7, 1–101.Google Scholar
Poinar, G. O. Jr. (1968). Parasitic development of Filipjevimermis leipsandra Poinar and Welch (Mermithidae) in Diabrotica u. undecimpuwtata (Chrysomelidae). Proceedings of the Helminthological Society of Washington 35, 161–9.Google Scholar
Poinar, G. O. Jr. (1969). Arthropod immunity to worms. In Immunity to Parasitic Animals, Vol. 1, pp. 173–210. Ed. Jackson, G. J., Herman, R. and Singer, I.New York: Meredith Corporation.Google Scholar
Poinar, G. O. Jr., Leutenegger, R. & Götz, P. (1968). Ultrastructure of the formation of a melanotic capsule in Diabrotica (Coleoptera) in response to a parasitic nematode (Mermithidae). Journal of Ultrastructure Research 25, 292–306.CrossRefGoogle ScholarPubMed
Poorbaugh, J. H., Anderson, J. R. & Burger, J. F. (1968). The insect inhabitants of undisturbed cattle droppings in Northern California. California Vector Views 15, 1–36.Google Scholar
Pouvreau, A. (1962). Contribution a l'etude de Sphaerularia bombi, parasite des reines do Bourdons. Annales de l'abeille 5, 181–99.CrossRefGoogle Scholar
Quintart, A. (1961). L'organe anal du larve de Drosophila melanogaster (Meig.). Annales de la société royale zoologique de Belgique 91, 117–28.Google Scholar
Ransom, B. H. (1913). The life history of Habronema muscae (Carter), a parasite of the horse transmitted by the house fly, pp. 1–36, No. 163. Washington, D.C.: Bulletin United States Bureau of Animal Industry.Google Scholar
Roubaud, E. & Descazeux, J. (1922). Deuxiemo contribution à l'etude des mouches, dans leurs rapports avec l'évolution des habronbèmes d'equidés. Bulletin de la Société de pathologie exotique 15, 978–1001.Google Scholar
Salt, G. (1963). The defence reactions of insects to metazoan parasites. Parasitology 53, 527–642.CrossRefGoogle ScholarPubMed
Sanders, D. P. & Dobson, R. C. (1966). The insect complex associated with bovine manure in Indiana. Annals of the Entomological Society of America 59, 955–9.CrossRefGoogle Scholar
Schacher, J. F. & Khalil, G. M. (1968). Development of Foleyella philistinae Schacher & Khalil, 1967 (Nematoda: Filarioidae) in Culex pipiens molestus with notes on pathology in the arthropod. Journal of Parasitology 54, 869–78.CrossRefGoogle ScholarPubMed
Schell, S. C. (1952). Tissue reactions of Blatella germanica L. to the developing larva of Physaloptera hispida Schell, 1950 (Nematoda: Spiruroidea). Transactions of the American Microscopical Society 71, 293–302.CrossRefGoogle Scholar
Shapiro, M. (1969). Immunity of insect hosts to insect parasites. In Immunity to Parasitic Animals, Vol. 1, pp. 173–210. Ed. Jackson, G. J., Herman, R. and Singer, I.. New York: Meredith Corporation.Google Scholar
Stoffolano, J. G. Jr. (1967). The synchronization of the life cycle of diapausing face flies, Musca autumnalis and of the nematode, Heterotylenchus autumnalis. Journal of Invertebrate Pathology 9, 395–7.CrossRefGoogle Scholar
Stoffolano, J. G. Jr. (1969). Nematode parasites of face fly and the onion maggot in France and Denmark. Journal of Economic Entomology 62, 792–5.CrossRefGoogle Scholar
Stoffolano, J. G. Jr. (1970). Experimental parasitization of Musca autumnalis De Geer, Musca domestica L., Orthellia caesarion Meig., and Ravinia l'herminieri R.-D. by the nematode Heterotylenchus autumnalis Nickle with special reference to host reactions, hemocytic involvement, anal organ, and the hemocytopoietic organ. pp. 177. Ph.D. Dissertation, Storrs: University of Connecticut.Google Scholar
Stoffolano, J. G. Jr. (1971). Darkening of the anal organ of larvae of Musca autumnalis and Orthellia caesarion when parasitized by the nematode Heterotylenchus autumnalis. Journal of Invertebrate Pathology 17, 3–8.CrossRefGoogle Scholar
Stoffolano, J. G. Jr. & Nickle, W. R. (1966). Nematode parasite (Heterotylenchus sp.) of face fly in New York State. Journal of Economic Entomology 59, 221–2.CrossRefGoogle Scholar
Taylor, R. (1969). A suggested role for the polyphenol-phenoloxidase system in invertebrate immunity. Journal of Invertebrate Pathology 14, 427–8.CrossRefGoogle ScholarPubMed
Treece, R. E. & Miller, T. A. (1968). Observations on Heterotylenchus autumnalis in relation to the face fly. Journal of Economic Entomology 61, 454–6.CrossRefGoogle Scholar
Vilagiova, I. (1968). Heterotylenchus autumnalis Nickle. (1967) — a parasite of pasture flies. Biólogia, Bratisl. 23, 397–400.Google ScholarPubMed
Wachek, F. (1955). Die entoparasitischen Tylenchiden. Parasitoligische Schriftenreihe 3, 1–119.Google Scholar
Welch, H. E. (1959). Taxonomy, life cycle, development, and habits of two new species of Allantonematidae (Nematoda) parasitic in drosophilid flies. Parasitology 49, 83–103.CrossRefGoogle ScholarPubMed
Welch, H. E. (1963). Nematode infections. In Insect Pathology, an Advanced Treatise, Vol. 2, pp. 363–92. Ed. Steinhaus, E. A.. New York: Academic Press.CrossRefGoogle Scholar
Welch, H. E. & Bronskill, J. F. (1962). Parasitism of mosquito larvae by the nematode, DD-136 (Nematoda: Neoaplectanidae). Canadian Journal of Zoology 40, 1263–8.CrossRefGoogle Scholar
West, L. S. (1951). The Housefly-Parasites, Predators, Symbionts and Commensals, pp. 1–584. Ithaca, New York: Comstock Publishing Company.Google Scholar
Wigglesworth, V. B. (1961). The tracheae and tracheoles of insects. Proceedings of the 11th International Congress of Entomology 1, 626–30.Google Scholar
Williams, P. (1961). Studies on Ethiopian Chrysops as possible vectors of loiasis. II. Chrysops silacea Austen and human loiasis. Annals of Tropical Medicine and Parasitology 55, 1–17.CrossRefGoogle ScholarPubMed
Wülker, G. (1923). Über Fortpflanzung und Entwicklung von Allantonema und verwandten Nematoden. Ergebnisse und Fortschritte der Zoologie, Jena 5, 389–507.Google Scholar
Yen, C. H. (1938). Studies on Dirofilaria immitis Leidy, with special reference to the susceptibility of some Minnesota species of mosquitoes to the infection. Journal of Parasitology 24, 189–205.CrossRefGoogle Scholar