Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T00:50:18.130Z Has data issue: false hasContentIssue false

Pathophysiology of Hymenolepis diminuta infections in Tenebrio molitor: effect of parasitism on haemolymph proteins

Published online by Cambridge University Press:  06 April 2009

Hilary Hurd
Affiliation:
Parasitology Research Laboratory, Department of Biological Sciences, University of Keele, Keele, Staffs. ST5 5BG
C. Arme
Affiliation:
Parasitology Research Laboratory, Department of Biological Sciences, University of Keele, Keele, Staffs. ST5 5BG

Summary

The effects of metacestodes of Hymenolepis diminuta on haemolymph proteins of Tenebrio molitor are restricted to female hosts. In beetles aged 15 days post-emergence, and harbouring 12-day-old metacestodes, haemolymph concentration is 46·7% higher than in non-infected animals and similar effects are found in longer standing infections. Electrophoresis of haemolymph revealed the presence of 13 bands. Densitometric analysis showed that only band 2/3 was significantly elevated in infected hosts although band 7/8 also showed an increase. These bands were also present in egg homogenates and are thought to be vitellogenins. It is therefore proposed that the excess protein found in infected beetles is a female-specific protein resulting from an interaction between the parasite and the host endocrine system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1984

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

Andreadis, T. G. & Hall, D. W. (1976). Neoaplectana carpocapsae: Encapsulation in Aedes aegypti and changes in host hemocytes and hemolymph proteins. Experimental Parasitology 39, 252–61.Google Scholar
Arai, H. P. (1980). Biology of the Tapeworm Hymenolepis diminuta. New York and London: Academic Press.Google Scholar
Arme, C. (1975). Tapeworm–host interactions. Symposium of the Society of Experimental Biology 29, 505–32.Google Scholar
Arme, C. & Coates, A. (1973). Hymenolepis diminuta: Active transport of α-aminoisobutyric acid by cysticercoid larvae. International Journal for Parasitology 3, 553–60.Google Scholar
Arme, C., Middleton, A. & Scott, J. P. (1973). Absorption of glucose and sodium acetate by cysticercoid larvae of Hymenolepis diminuta. Journal of Parasitology 59, 214.Google Scholar
Arme, C., Bridges, J. & Hoole, D. (1983). Pathology of cestode infections in the vertebrate host. In Biology of the Eucestoda, vol. 2 (ed. Arme, C. and Pappas, P. W), pp. 499538. London and New York: Academic Press.Google Scholar
Chambers, S. P., Hall, J. E. & Hitt, S. Z. (1975). Effects of trematode infections on the haemolymph of aquatic insects. Journal of Invertebrate Pathology 25, 171–7.CrossRefGoogle Scholar
Fioravanti, C. F. & MacInnis, A. J. (1977). The identification and characterization of a prenoid constituent (farnesol) of Hymenolepis diminuta (Cestoda). Comparative Biochemistry and Physiology 57B, 227–33.Google Scholar
Frayha, G. J. & Fairbairn, D. (1969). Lipid metabolism in belminth parasites – VI. Synthesis of 2-cis, 6-trans farnesol by Hymenolepis diminuta (Cestoda). Comparative Biochemistry and Physiology 28, 1115–24.Google Scholar
Freeman, R. S. (1983). Pathology of the invertebrate host–metacestode relationship. In Biology of the Eucestoda, vol. 2 (ed. Arme, C. and Pappas, P. W.), pp. 441–98. London and New York: Academic Press.Google Scholar
Gordon, R., Condon, W. J., Edgar, W. J. & Babie, S. J. (1978). Effects of mermithid parasitism on the haemolymph composition of the larval blackflies Prosimulium mixtum/fuscum and Simulium venustum. Parasitology 77, 367–74.Google Scholar
Gordon, R., Webster, J. M. & Hislop, T. G. (1973). Mermithid parasitism, protein turnover and vitellogenesis in the Desert Locust, Schistocercagregaria Forskal. Comparative Biochemistry and Physiology 46B, 575–93.Google Scholar
Hagedorn, H. H. & Kunkel, J. G. (1979). Vitellogenin and vitellin in insects. Annual Review Entomology 24, 475505.CrossRefGoogle Scholar
Harnish, D. G. & White, B. N. (1982). Insect vitellins: Identification, purification and characterization from eight orders. Journal of Experimental Zoology 220, 110.CrossRefGoogle Scholar
Hurd, H. & Arme, C. (1982). Hymenolepis diminuta: the pathophysiology of infection in the intermediate host, Tenebrio molitor. Parasitology 85, lxii.Google Scholar
Hurd, H. & Arme, C. (1983). The pathophysiology of Hymenolepis diminuta infections in Tenebrio molitor. Parasitology 87, lxvii.Google Scholar
Hurd, H. & Arme, C. (1984). Tenebrio molitor (Coleoptera): effect of metacestodes of Hymenolepis diminuta (Cestoda) on haemolymph amino acids. Parasitology 89, 245251.CrossRefGoogle Scholar
Jeffs, S. & Arme, C. (1982). Hymenolepis diminuta: uptake of amino acids by cysticercoid larvae. Parasitology 85, xxiv.Google Scholar
Jeffs, S. & Arme, C. (1984). Hymenolepis diminuta: protein synthesis in cysticercoids. Parasitology 88, 351–7.CrossRefGoogle Scholar
Keymer, A. (1980). The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum. Parasitology 81, 405–21.CrossRefGoogle ScholarPubMed
Keymer, A. (1981). Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 50, 941–50.CrossRefGoogle Scholar
Laverdure, A.-M. (1972). L'evolution de l'ovarie chez la femelle adulte de Tenebrio molitor – La vitellogeniese. Journal of Insect Physiology 18, 1369–85.CrossRefGoogle Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–75.CrossRefGoogle ScholarPubMed
Mankau, S. K. (1977). Sex as a factor in infection of Tribolium spp. by Hymenolepis diminuta. Environmental Entomology 6, 2.CrossRefGoogle Scholar
Mettrick, D. F. (1980). The intestine as an environment. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 281356. New York and London: Academic Press.Google Scholar
Mettrick, D. F. (1982). Behavioural and physiological cues of cestodes, with particular reference to serotonin (5-HT). In Cues that Influence Behaviour of Internal Parasites (ed. Bailey, W. S.), pp. 85109. New Orleans: US Department of Agriculture.Google Scholar
Mordue, W. (1965). Neuro-endocrine factors in the control of oocyte production in Tenebrio molitor L. Journal of Insect Physiology 11, 617–29.CrossRefGoogle Scholar
Pappas, P. W. (1983). Host–parasite interface. In Biology of the Eucestodz vol. 2 (ed. Arme, C. and Pappas, P. W.), pp. 297334. London: Academic Press.Google Scholar
Pembrick, S. M. & Butz, A. (1970). Common electrophoretic properties of the fat body, haemolymph, and oocytes of adult Tenebrio molitor. Journal of Insect Physiology 16, 1443–53.CrossRefGoogle Scholar
Phillips, A. A. & Arme, C. (1983). Hymenolepis diminuta: transport of monosaccharides by cysticercoids. Parasitology 87, lxiii.Google Scholar
Richards, K. S. & Arme, C. (1983). The rostellar tegumentary cytoplasm of the metacestode of Hymenolepis diminuta (Cyclophyllidea: Cestoda). Parasitology 86, 83–8.Google Scholar
Schmidt, S. P. & Platzer, E. G. (1980). An investigation of possible Romanomermis culicivorax proteins in the haemolymph of Culex pipiens. Journal of Invertebrate Pathology 36, 149–58.CrossRefGoogle ScholarPubMed
Soltice, G., Arai, H. P. & Scheinberg, E. (1971). Host parasite interactions of Tribolium confusum and Tribolium castaneum with Hymenolepis diminuta. Canadian Journal of Zoology 49, 265–73.CrossRefGoogle ScholarPubMed
Sroka, P. & Vinson, S. B. (1978). Phenoloxidase activity in the haemolymph of parasitized and unparasitized Heliothis virescens. Insect Biochemistry 8, 399402.CrossRefGoogle Scholar
Strambi, C., Strambi, A. & Augier, R. (1982). Protein level in the haemolymph of the wasp Polistes gallicus L. at the beginning of imaginal life and during overwintering. Action of the streptsipterian parasite Xenos vesparum Rossi. Experientia 38, 1189–91.CrossRefGoogle Scholar
Telfer, W. H. (1954). Immunological studies of insect metamorphosis. II. The role of a sex-linked blood protein in egg formation by the Cecropia silkworm. Journal of General Physiology 37, 539–58.Google Scholar
Thong, C. H. S. & Webster, J. M. (1975). Effects of Contortylenchus reversus (Nematoda: sphaerularridae) on haemolymph composition and oocyte development in the beetle Dendroctonus pseudotsugae (Coleoptera: scolytidae). Journal of Invertebrate Pathology 26, 91–8.CrossRefGoogle ScholarPubMed
Wang, C.-M. & Patton, R. L. (1968). The separation and characterization of the haemolymph proteins of several insects. Journal of Insect Physiology 14, 1069–75.Google Scholar
Weber, K. & Osborn, M. (1969). The reliability of molecular weight determination by dodecyl sulphate-polyacrylamide gel electrophoresis. Journal of Biological Chemistry 244, 4406–12.Google Scholar
Womersley, C. & Platzer, E. G. (1982). The effect of parasitism by the mermithid Romanomermis culicivorax on the dry weight and haemolymph soluble protein content of three species of mosquitoes. Journal of Invertebrate Pathology 40, 406–12.CrossRefGoogle ScholarPubMed
Wyatt, G. R. & Pan, M. L. (1978). Insect plasma proteins. Annual Review of Biochemistry 47, 779818.CrossRefGoogle ScholarPubMed
Zacharius, R. M., Zell, T. E., Morrison, J. H. & Woodlock, J. J. (1969). Glycoprotein staining following electrophoresis on acrylamide gels. Analytical Biochemistry 30, 148–52.CrossRefGoogle ScholarPubMed