Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-22T11:31:26.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of the effects of multiple variables on the levels of infection of the rat tapeworm, Hymenolepis diminuta, in its intermediate host, the confused flour beetle Tribolium confusum

Published online by Cambridge University Press:  14 January 2020

A. Yezerski Open the ORCID record for A. Yezerski [Opens in a new window] ,
Y. Luyten  and
T. Dubiel
A. Yezerski*
Affiliation:
Biology Department, University of Vermont, Marsh Life Science Building, Burlington, VT05405, USA
Y. Luyten
Affiliation:
Biology Department, University of Vermont, Marsh Life Science Building, Burlington, VT05405, USA
T. Dubiel
Affiliation:
Biology Department, University of Vermont, Marsh Life Science Building, Burlington, VT05405, USA
*
Author for correspondence: A. Yezerski, E-mail: annyezerski@kings.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

The interaction of the rat tapeworm, Hymenolepis diminuta, with its intermediate beetle host, Tribolium confusum, is a well-studied model system. However, there is so much variation in the methods and designs of the studies that it is difficult to draw comparisons. This study simultaneously compared several aspects of the infection protocol including beetle age, sex, density and mating status; parasite egg condition, infection environment humidity and the times for the three steps of infection: starvation, feeding and post-feeding development. Although statistically limited by low prevalence and intensity levels, we were able to detect the relative effects of the variables. The effects of these variables on prevalence (percent infection) and intensity (mean number of cysticercoids) do not necessarily correlate with each other. Egg condition, reduced starvation times, higher beetle density and longer development times reduced prevalence. However, differences in intensity were only detected with older beetles. When coupled with survivorship data, our study found that our current infection protocol is optimal for infection success. However, the results suggest extending the study to other intermediate hosts and the inclusion of additional variables.

Keywords

Tribolium confusumHymenolepis diminutacysticercoidinfection protocolsusceptibility
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e116
Copyright
Copyright © Cambridge University Press 2020

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.)

Footnotes

*

Current address: Ann Yezerski, King's College, Biology Department, 133 North River Street, Wilkes-Barre, PA 18711, USA

†

Current address: Yvette Luyten, New England Biolabs, 240 County Road, Ipswich, MA 01938-2723, USA

‡

Current address: Trajan Dubiel, Michigan State University, 404 Wilson Road, Room 201, East Lansing, MI 48824, USA

References

Carver, FJ and Hurd, H (1998) The effect of metacestodes of Hymenolepis diminuta on the bean-shaped accessory glands in male Tenebrio molitor. Parasitology 116(Pt 2), 191–196.CrossRefGoogle ScholarPubMed
Chin, HM, Luong, LT and Shostak, AW (2017) Rehydration methods to recover cysticercoids of the rat tapeworm Hymenolepis diminuta from dry flour beetle carcasses. Journal of Helminthology 91, 470–478.CrossRefGoogle ScholarPubMed
Cole, TJ, Eggleston, P and Hurd, H (2003) Juvenile hormone titre and egg production in Tenebrio molitor infected by Hymenolepis diminuta: effect of male and/or female infection, male age and mating. Journal of Insect Physiology 49, 583–590.CrossRefGoogle ScholarPubMed
Drnevich, JM, Papke, RS, Rauser, CL and Rutowski, RL (2001) Material benefits from multiple mating in female mealworm beetles (Tenebrio molitor L.). Journal of Insect Behavior 14, 215–230.CrossRefGoogle Scholar
Dunkley, LC and Mettrick, DF (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, WS 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
Granath, WO Jr (1980) Hymenolepis diminuta (Cestoda): effects of parasite density and temperature on the water balance of Tenebrio molitor and subsequent infectivity of the cysticercoids. Journal of Invertebrate Pathology 36, 235–239.CrossRefGoogle ScholarPubMed
Hangartner, S, Sbilordo, SH, Michalczyk, L, Gage, MJ and Martin, OY (2013) Are there genetic trade-offs between immune and reproductive investments in Tribolium castaneum? Infection, Genetics and Evolution 19, 45–50.CrossRefGoogle ScholarPubMed
Hangartner, S, Michalczyk, L, Gage, MJ and Martin, OY (2015) Experimental removal of sexual selection leads to decreased investment in an immune component in female Tribolium castaneum. Infection, Genetics and Evolution 33, 212–218.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
Hitchen, SJ, Shostak, AW and Belosevic, M (2009) Hymenolepis diminuta (Cestoda) induces changes in expression of select genes of Tribolium confusum (Coleoptera). Parasitology Research 105, 875–879.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 B: Biological Sciences 270(2), S172–S174.CrossRefGoogle ScholarPubMed
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: effect of infection upon the potency of the follicular epithelium in the intermediate host, Tenebrio molitor. Journal of Invertebrate Pathology 49, 227–234.CrossRefGoogle Scholar
Kelly, RJ, O'Brien, DM and Katz, FF (1967) The incidence and burden of Hymenolepis diminuta cysticercoids as a function of the age of the intermediate host, Tribolium confusum. Journal of the New York Entomological Society 75, 19–23.Google Scholar
Kerstes, NA and Martin, OY (2014) Insect host-parasite coevolution in the light of experimental evolution. Insect Science 21, 401–414.CrossRefGoogle ScholarPubMed
Kerstes, NA, Berenos, C and Martin, OY (2013) Coevolving parasites and population size shape the evolution of mating behaviour. BMC Evolutionary Biology 13, 29.CrossRefGoogle ScholarPubMed
Keymer, AE (1980) The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host Tribolium confusum. Parasitology 81, 405–421.CrossRefGoogle ScholarPubMed
Keymer, AE (1981) Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 50, 941–950.CrossRefGoogle Scholar
Keymer, A (1982) The dynamics of infection of Tribolium confusum by Hymenolepis diminuta: the influence of exposure time and host density. Parasitology 84, 157–166.CrossRefGoogle ScholarPubMed
Keymer, AE and Anderson, RM (1979) The dynamics of infection of Tribolium confusum by Hymenolepis diminuta: the influence of infective-stage density and spatial distribution. Parasitology 79, 195–207.CrossRefGoogle ScholarPubMed
Lackie, AM (1976) Evasion of the haemocytic defence reaction of certain insects by larvae of Hymenolepis diminuta (Cestoda). Parasitology 73, 97–107.CrossRefGoogle Scholar
Lethbridge, RC (1971a) The hatching of Hymenolepis diminuta eggs and penetration of the hexacanths in Tenebrio molitor beetles. Parasitology 62, 445–456.CrossRefGoogle Scholar
Lethbridge, RC (1971b) An improved gradient centrifugation technique for the separation of Hymenolepis diminuta eggs from rat feces. The Journal of Parasitology 57, 1140–1142.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
Maki, J and Yanagisawa, T (1987) Infectivity of Hymenolepis nana eggs from faecal pellets in the rectum of mice. Journal of Helminthology 61, 341–345.CrossRefGoogle Scholar
Mankau, SK (1971) Host sex effects on infection of Tribolium confusum by Hymenolepis diminuta. Tribolium Information Bulletin 14, 82–83.Google Scholar
Mankau, SK (1977) Sex as a factor in the infection of Tribolium spp. by Hymenolepis dimimnuta. Environmental Entomology 6, 233–236.CrossRefGoogle Scholar
Maya, C, Ortiz, M and Jimenez, B (2010) Viability of Ascaris and other helminth genera non larval eggs in different conditions of temperature, lime (pH) and humidity. Water Science and Technology 62, 2616–2624.CrossRefGoogle ScholarPubMed
Oldham, JN (1931) On the arthropod intermediate hosts of Hymenolepis diminuta (Rudolphi 1819). Journal of Helminthology 9, 21–28.CrossRefGoogle Scholar
Pai, A and Yan, G (2003) Effects of tapeworm infection on male reproductive success and mating vigor in the red flour beetle, Tribolium castaneum. Journal of Parasitology 89, 516–521.CrossRefGoogle ScholarPubMed
Pappas, PW and Morrison, SE (1995) Benzoquinones of the beetles, Tribolium castaneum and Tribolium confusum. Preparative Biochemistry 25, 155–168.CrossRefGoogle ScholarPubMed
Pappas, PW, Marschall, EA, Morrison, SE, Durka, GM and Daniel, CS (1995) Increased coprophagic activity of the beetle, Tenebrio molitor, on feces containing eggs of the tapeworm, Hymenolepis diminuta. International Journal for Parasitology 25, 1179–1184.CrossRefGoogle ScholarPubMed
Park, T, Mertz, DB and Petrusewicz, K (1961) Genetic strains of Tribolium: their primary characteristics. Physiological Zoology 34, 289–321.CrossRefGoogle Scholar
Rau, ME (1979) The frequency of the distribution of Hymenolepis diminuta cysticercoids in natural, sympatric populations of Tenebrio molitor and T. obscurus. International Journal for Parasitology 9, 85–97.CrossRefGoogle Scholar
Richards, KS and Arme, C (1985) Phagocytosis of microvilli of the metacestode of Hymenolepis diminuta by Tenebrio molitor haemocytes. Parasitology 90, 365–374.CrossRefGoogle Scholar
Ridley, M (1988) Mating frequency and fecunity in insects. Biological Reviews 63, 509–549.CrossRefGoogle Scholar
Sall, J, Creighton, L and Lehman, A (2006) JMP start statistics. 3rd edn. 560 pp. Cary, NC, Thomson Learning.Google Scholar
Shea, JF (2005) Sex differences in frass production and weight change in Tenebrio molitor (Coleoptera) infected with cysticercoids of the tapeworm Hymenolepis diminuta (Cestoda). Journal of Insect Science 5, 31.CrossRefGoogle Scholar
Shostak, AW (2008) Effect of age of the intermediate host Tribolium confusum (Coleoptera) on infection by Hymenolepis diminuta (Cestoda). Journal of Parasitology 94, 152–157.CrossRefGoogle Scholar
Shostak, AW (2012) Sequential and concurrent exposure of flour beetles (Tribolium confusum) to tapeworms (Hymenolepis diminuta) and pesticide (diatomaceous earth). Journal of Parasitology 98, 453–459.CrossRefGoogle Scholar
Shostak, AW (2014) Hymenolepis diminuta infections in tenebrionid beetles as a model system for ecological interactions between helminth parasites and terrestrial intermediate hosts: a review and meta-analysis. Journal of Parasitology 100, 46–58.CrossRefGoogle ScholarPubMed
Shostak, AW, Walsh, JG and Wong, YC (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 Scholar
Shostak, AW, Walsh, JG and Wong, YC (2008) Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum. Parasitology 135, 1019–1033.CrossRefGoogle ScholarPubMed
Shostak, AW, Van Buuren, KG and Cook, R (2015) Response of flour beetles to multiple stressors of parasitic (Hymenolepis diminuta), environmental (diatomaceous earth), and host (reproduction) origin. Journal of Parasitology 101, 405–417.CrossRefGoogle ScholarPubMed
Siles-Lucas, M and Hemphill, A (2002) Cestode parasites: application of in vivo and in vitro models for studies on the host-parasite relationship. Advances in Parasitology 51, 133–230.CrossRefGoogle ScholarPubMed
Sokoloff, A (1972) The biology of Tribolium with special emphasis on genetic aspects. 300 pp. Oxford, Clarendon Press.Google Scholar
Soltice, GE, Arai, HP and Scheinberg, E (1971) Host-parasite intereaction of Tribolium confusum and Tribolium castaneum with Hymenolepis diminuta. Canadian Journal of Zoology 49, 265–273.CrossRefGoogle Scholar
Stevens, L, Guiyun, Y and Pray, LA (1997) Consequences of inbreeding on invertebrate host susceptibility to parasite infection. Evolution; International Journal of Organic Evolution 51, 2032–2039.CrossRefGoogle Scholar
Turner, JA and Voge, M (1956) Effect of temperature on larval development of the cestode, Hymenolepis diminuta. Experimental Parasitology 5, 580–586.Google ScholarPubMed
Voge, M (1959a) Sensitivity of developing Hymenolepis diminuta larvae to high temperature stress. Journal of Parasitology 45, 175–181.CrossRefGoogle Scholar
Voge, M (1959b) Temperature stress and development of Hymenolepis diminuta in Tribolium confusum on different diets. Journal of Parasitology 45, 591–596.CrossRefGoogle Scholar
Worden, BD and Parker, P (2005) Females prefer non-infected males as mates in the grain beetle Tenebrio molitor: evidence in pre- and postcopulatory behaviors. Animal Behavior 70, 1047–1053.CrossRefGoogle Scholar
Yan, G (1997) Consequences of larval tapeworm infection for the fitness of the intermediate hosts, flour beetles (Tribolium spp.). Canadian Journal of Zoology 75, 271–279.CrossRefGoogle Scholar
Yan, G and Norman, S (1995) Infection of Tribolium beetles with a tapeworm: variation in susceptibility within and between beetle species and among genetic strains. Journal of Parasitology 81, 37–42.CrossRefGoogle ScholarPubMed
Yan, G and Phillips, TW (1996) Influence of tapeworm infection on the production of aggregation pheromone and defensive compounds in Tribolium castaneum. Journal of Parasitology 82, 1037–1039.CrossRefGoogle ScholarPubMed
Yan, G, Stevens, L and Schall, JJ (1994) Behavioral changes in Tribolium beetles infected with a tapeworm: variation in effects between beetle species and among genetic strains. American Naturalist 143, 830–847.CrossRefGoogle Scholar
Yezerski, A (2001) Benzoquinones in Tribolium beetles: the genetics and ecology of defense. in Raikel, AS, James, AA, Christiansen, BM, French-Constant, R and O'Brochta, DA (Eds) Genetic manipulation of insects. Taos, New Mexico, Keystone Symposia, 58.Google Scholar
Yezerski, A, Gilmor, TP and Stevens, L (2000) Variation in the production and distribution of substituted benzoquinone compounds among genetic strains of the confused flour beetle, Tribolium confusum. Physiological and Biochemical Zoology 73, 192–199.CrossRefGoogle ScholarPubMed
Yezerski, A, Stevens, L and Ametrano, J (2003) A genetic linkage map for Tribolium confusum based on Random Amplified Polymorphic DNA's (RAPD's) and Recombinant Inbred (RI) lines. Insect Molecular Biology 12, 517–526.CrossRefGoogle Scholar
Yezerski, A, Ciccone, C, Rozitski, J and Volingavage, B (2007) The effects of a naturally produced benzoquinone on microbes common to flour. Journal of Chemical Ecology 33, 1217–1225.CrossRefGoogle ScholarPubMed
Zhong, D, Pai, A and Yan, G (2003) Quantitative trait loci for susceptibility to tapeworm infection in the red flour beetle. Genetics 165, 1307–1315.Google ScholarPubMed
Zhong, D, Pai, A and Yan, G (2005) Costly resistance to parasitism: evidence from simultaneous quantitative trait loci mapping for resistance and fitness in Tribolium castaneum. Genetics 169, 2127–2135.CrossRefGoogle ScholarPubMed