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Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum

Published online by Cambridge University Press:  12 May 2008

A. W. SHOSTAK ,
J. G. WALSH  and
Y. C. WONG
A. W. SHOSTAK*
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Building, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
J. G. WALSH
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Building, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
Y. C. WONG
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Building, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
*
*Corresponding author: Tel: 011 1 780 492 1293. Fax: 011 1 780 492 9234. E-mail: [email protected]
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Summary

We studied the ‘crowding effect’ in Tribolium confusum infected with Hymenolepis diminuta. Manipulations included age and number of parasites, and diet, sex, age and number of exposures of hosts. Volume per parasite was unaffected until an intensity of at least 5–10 parasites per host, then declined approximately inversely as intensities increased. Parasite size was affected by host sex but not age or reproductive status. Host diet affected parasite size and the impact of crowding. Daily gain in parasite volume peaked partway through the developmental period and preceded the first evidence of a crowding effect. Parasites that established during a second exposure had a transient developmental delay but eventually grew as large or larger than parasites from a single exposure with the same total intensity. Parasites responded to crowding by differential allocation of resources. Cercomer volume decreased even with slight crowding, the capsule surrounding the scolex was not reduced until crowding became more severe, and scolex width was reduced only in the most extreme conditions. The data support the hypothesis that the crowding effect in this system is driven primarily by nutrient, rather than space limitations.

Keywords

Hymenolepis diminutaTribolium confusumcrowding effectdensity-dependencedevelopmentgrowthhost diet
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 8 , July 2008 , pp. 1019 - 1033
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Arme, C., Middleton, A. and Scott, J. P. (1973). Absorption of glucose and sodium acetate by cysticercoid larvae of Hymenolepis diminuta. Journal of Parasitology 59, 214.CrossRefGoogle ScholarPubMed
Boggs, C. L. (1992). Resource allocation: exploring connections between foraging and life history. Functional Ecology 6, 508–518.CrossRefGoogle Scholar
Brown, S. P., De Lorgeril, J., Joly, C. and Thomas, F. (2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668–672.CrossRefGoogle ScholarPubMed
Bush, A. O. and Lotz, J. M. (2000). The ecology of ‘crowding’. Journal of Parasitology 86, 212–213.Google ScholarPubMed
Chervy, L. (2002). The terminology of larval cestodes or metacestodes. Systematic Parasitology 52, 1–33.CrossRefGoogle Scholar
Dunkley, L. C. and Mettrick, D. F. (1971). Factors affecting the susceptibility of the beetle Tribolium confusum to infection by Hymenolepis diminuta. Journal of the New York Entomological Society 79, 133–138.Google Scholar
Evans, W. S. and Novak, M. (1976). The effect of mebendazole on the development of Hymenolepis diminuta in Tribolium confusum. Canadian Journal of Zoology 54, 1079–1083.CrossRefGoogle ScholarPubMed
Fredensborg, B. L. and Poulin, R. (2005). Larval helminths in intermediate hosts: Does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061–1070. doi: 10.1016/j.ijpara.2005.05.005CrossRefGoogle ScholarPubMed
Gordon, D. M. and Whitfield, P. J. (1985). Interactions of the cysticercoids of Hymenolepis diminuta and Raillietina cesticillus in their intermediate host, Tribolium confusum. Parasitology 90, 421–431.CrossRefGoogle ScholarPubMed
Heins, D. C., Baker, J. A. and Martin, H. C. (2002). The ‘crowding effect’ in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302–307.Google ScholarPubMed
Heyneman, D. and Voge, M. (1957). Glycogen distribution in cysticercoids of three hymenolepid cestodes. Journal of Parasitology 43, 527–531.CrossRefGoogle Scholar
Heyneman, D. and Voge, M. (1971). Host response of the flour beetle, Tribolium confusum, to infections with Hymenolepis diminuta, H. microstoma, and H. citelli (Cestoda: Hymenolepididae). Journal of Parasitology 57, 881–886.CrossRefGoogle Scholar
Hurd, H. and Ardin, R. (2003). Infection increases the value of nuptial gifts, and hence male reproductive success, in the Hymenolepis diminuta – Tenebrio molitor association. Proceedings of the Royal Society of London, B 270, S172–S174.CrossRefGoogle ScholarPubMed
Hurd, H. and Arme, C. (1984 a). Pathophysiology of Hymenolepis diminuta infections in Tenebrio molitor: effect of parasitism on haemolymph proteins. Parasitology 89, 253–262.CrossRefGoogle Scholar
Hurd, H. and Arme, C. (1984 b). Tenebrio molitor (Coleoptera): effect of metacestodes of Hymenolepis diminuta (Cestoda) on haemolymph amino acids. Parasitology 89, 245–251.CrossRefGoogle Scholar
Hurd, H. and Arme, C. (1986). Hymenolepis diminuta: effect of metacestodes on production and viability of eggs in the intermediate host, Tenebrio molitor. Journal of Invertebrate Pathology 47, 225–230.CrossRefGoogle ScholarPubMed
Hurd, H. and Arme, C. (1987). Hymenolepis diminuta (Cestoda): the role of intermediate host sex in the establishment, growth and development of metacestodes in Tenebrio molitor (Coleoptera). Helminthologia 24, 23–31.Google Scholar
Jeffs, S. A. and Arme, C. (1984). Hymenolepis diminuta: protein synthesis in cysticercoids. Parasitology 88, 351–357.CrossRefGoogle Scholar
Kearns, J. Y., Hurd, H. and Pullin, A. S. (1994). Effect of metacestodes of Hymenolepis diminuta on storage and circulating carbohydrates in the intermediate host, Tenebrio molitor. Parasitology 108, 473–478.CrossRefGoogle ScholarPubMed
Keymer, A. (1980). The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum. Parasitology 81, 405–421.CrossRefGoogle ScholarPubMed
Keymer, A. (1981). Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 50, 941–950.CrossRefGoogle Scholar
Maema, M. (1986). Experimental infection of Tribolium confusum (Coleoptera) by Hymenolepis diminuta (Cestoda): host fecundity during infection. Parasitology 92, 405–412.CrossRefGoogle ScholarPubMed
Major, M., Webb, T. J. and Hurd, H. (1997). Haemolymph from female beetles infected with Hymenolepis diminuta metacestodes retards the development of ovarian follicles in recipient Tenebrio molitor. Parasitology 114, 175–179.CrossRefGoogle ScholarPubMed
Mankau, S. K. (1977). Sex as a factor in the infection of Tribolium spp. by Hymenolepis diminuta. Environmental Entomology 6, 233–236.CrossRefGoogle Scholar
Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: Experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 39–57. doi: 10.1007/s10682-005-3274-3270.CrossRefGoogle Scholar
Moczon, T. (1977). Glycogen distribution and the accumulation of radioactive compounds in oncospheres and cysticercoids of Hymenolepis diminuta (Cestoda) after incubation in glucose-14C1–6. Acta Parasitologica Polonica 24, 269–274.Google Scholar
Novak, M., Modha, A. and Blackburn, B. J. (1993). D-[1-13C]Glucose metabolism of Tribolium confusum parasitized by hymenolepid metacestodes. Journal of Invertebrate Pathology 62, 302–307.CrossRefGoogle Scholar
Pappas, P. W. and Morrison, S. E. (1995). Hymenolepis diminuta metacestodes (cysticercoids) are unable to utilize exogenous trehalose. Journal of Parasitology 81, 652–653.CrossRefGoogle ScholarPubMed
Prescott, D. M. and Voge, M. (1959). Autoradiographic study of the synthesis of ribonucleic acid in cysticercoids of Hymenolepis diminuta. Journal of Parasitology 45, 587–590.CrossRefGoogle ScholarPubMed
Read, C. P. (1951). The ‘crowding effect’ in tapeworm infections. Journal of Parasitology 37, 174–178.CrossRefGoogle ScholarPubMed
Roberts, L. S. (1980). Development of Hymenolepis diminuta in its definitive host. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 357–423. Academic Press, New York.CrossRefGoogle Scholar
Roberts, L. S. (2000). The crowding effect revisited. Journal of Parasitology 86, 209–211.Google ScholarPubMed
Roberts, L. S. and Insler, G. D. (1982). Developmental physiology of cestodes. XVII. Some biological properties of putative ‘crowding factors’ in Hymenolepis diminuta. Journal of Parasitology 68, 263–269.CrossRefGoogle ScholarPubMed
Rosen, R. and Uglem, G. L. (1988). Localization of facilitated diffusion and active glucose transport in cysticercoids of Hymenolepis diminuta (Cestoda). International Journal for Parasitology 18, 581–584.CrossRefGoogle ScholarPubMed
Schoen, J., Modha, A., Maslow, K., Novak, M. and Blackburn, B. J. (1996). A NMR study of parasitized Tenebrio molitor and Hymenolepis diminuta cysticercoids. International Journal for Parasitology 26, 713–722.CrossRefGoogle ScholarPubMed
Shea, J. F. (2005). Sex differences in frass production and weight change in Tenebrio molitor (Colepotera) infected with cysticercoids of the tapeworm Hymenolepis diminuta (Cestoda). Journal of Insect Science 5.31, 1–6. DOI: 10.1673/1536-2442 (2005)5[1:SDIFPA]2.0.CO;2Google Scholar
Shostak, A. W. (2008). Effect of age of the intermediate host Tribolium confusum (Coleoptera) on infection by Hymenolepis diminuta (Cestoda). Journal of Parasitology 94, 152–157.CrossRefGoogle ScholarPubMed
Shostak, A. W., Rosen, R. B. and Dick, T. A. (1985). The use of growth curves to assess the crowding effect on procercoids of the tapeworm Triaenophorus crassus in the copepod host Cyclops bicuspidatus thomasi. Canadian Journal of Zoology 63, 2343–2351.CrossRefGoogle Scholar
Shostak, A. W. and Scott, M. E. (1993). Detection of density-dependent growth and fecundity of helminths in natural infections. Parasitology 106, 527–539.CrossRefGoogle ScholarPubMed
Shostak, A. W., Walsh, J. G. and Wong, Y. C. (2006). Shape variation of cysticercoids of Hymenolepis diminuta (Cyclophyllidea) from fed, partially fed and fasted Tribolium confusum (Coleoptera). Journal of Parasitology 92, 756–763.CrossRefGoogle ScholarPubMed
Voge, M. and Heyneman, D. (1957). Development of Hymenolepis nana and Hymenolepis diminuta (Cestoda: Hymenolepididae) in the intermediate host Tribolium confusum. University of California Publications in Zoology 59, 549–579.Google Scholar
Warr, E., Eggleston, P. and Hurd, H. (2004). Apoptosis in the fat body tissue of the beetle Tenebrio molitor parasitised by Hymenolepis diminuta. Journal of Insect Physiology 50, 1037–1043.CrossRefGoogle ScholarPubMed
Webb, T. J. and Hurd, H. (1999). Direct manipulation of insect reproduction by agents of parasite origin. Proceedings of the Royal Society of London, B 266, 1537–1541.CrossRefGoogle Scholar