Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-19T11:17:12.389Z Has data issue: false hasContentIssue false
  • English
  • Français

Behavioural changes in the flour beetle Tribolium confusum infected with the spirurid nematode Protospirura muricola

Published online by Cambridge University Press:  10 September 2013

M. Schutgens ,
B. Cook ,
F. Gilbert  and
J.M. Behnke
M. Schutgens
Affiliation:
School of Biology, University of Nottingham, University Park, NottinghamNG7 2RD, UK
B. Cook
Affiliation:
School of Biology, University of Nottingham, University Park, NottinghamNG7 2RD, UK
F. Gilbert
Affiliation:
School of Biology, University of Nottingham, University Park, NottinghamNG7 2RD, UK
J.M. Behnke*
Affiliation:
School of Biology, University of Nottingham, University Park, NottinghamNG7 2RD, UK
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

We examined changes to the behaviour of flour beetles, Tribolium confusum, infected with the rodent stomach worm, the spirurid Protospirura muricola, in the context of the ‘Behavioural Manipulation Hypothesis’. Trobolium confusum infected with the third-stage infective larvae of P. muricola showed consistently altered patterns of behaviour. Relative to uninfected beetles, over a measured time period, beetles infected with P. muricola were likely to move over a shorter distance, when moving their speed of movement was slower, they were more likely to stay in the illuminated area of their environment, more likely to emerge from darkened areas into the illuminated areas, and their longevity was significantly shortened. The changes in behaviour, as reflected in effects on speed of movement, were only evident among beetles that actually harboured infective cysts and not among those carrying younger infections when the larvae within their haemocoels would have been at an earlier stage of development and not yet capable of infecting the definitive murine hosts. We discuss whether these changes would have made the beetles more susceptible to predation by rodents, and specifically by the omnivorous eastern spiny mouse, Acomys dimidiatus, the natural definitive host of this parasite in Egypt, from where the P. muricola isolate originated, and whether they support the Behavioural Manipulation Hypothesis or reflect parasite-induced pathology.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 1 , January 2015 , pp. 68 - 79
Copyright
Copyright © Cambridge University Press 2013 

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

Barber, I., Hoare, D. & Krause, J. (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10, 131–165.Google Scholar
Barnard, C.J. & Behnke, J.M. (1990) Parasitism and host behaviour. London, UK, Taylor & Francis.Google Scholar
Barnard, C., Gilbert, F. & McGregor, P. (2007) Asking questions in biology. 3rd edn.London, Prentice Hall.Google Scholar
Bauer, A., Haine, E.R., Perrot-Minnot, M.-J. & Rigaud, T. (2005) The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipods hosts: the native Gammarus pulex and the invasive Gammarus roeseli. Journal of Zoology 267, 39–43.CrossRefGoogle Scholar
Baylis, H.A. (1928) On a collection of nematodes from Nigerian mammals (chiefly rodents). Parasitology 20, 280–304.Google Scholar
Behnke, J.M., Barnard, C.J., Mason, N., Harris, P.D., Sherif, N.E., Zalat, S. & Gilbert, F.S. (2000) Intestinal helminths of spiny mice (Acomys cahirinus dimidiatus) from St Katherine's Protectorate in the Sinai, Egypt. Journal of Helminthology 74, 31–44.Google Scholar
Behnke, J.M., Harris, P.D., Bajer, A., Barnard, C.J., Sherif, N., Cliffe, L., Hurst, J., Lamb, M., Rhodes, A., James, M., Clifford, S., Gilbert, F.S. & Zalat, S. (2004) Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St. Katherine region of the Sinai Peninsula in Egypt. Parasitology 129, 379–398.CrossRefGoogle ScholarPubMed
Bethel, W.M. & Holmes, J.C. (1973) Altered evasive behaviour and responses to light in amphipods harbouring acanthocephalan cystacanths. Journal of Parasitology 59, 945–954.CrossRefGoogle Scholar
Bethel, W.M. & Holmes, J.C. (1974) Correlation of development of altered evasive behaviour in Gammarus lacustris (Amphipoda) harbouring cystacanths of Polymorphus paradoxus (Acanthocephala) with the infectivity to the definitive host. Journal of Parasitology 60, 272–274.Google Scholar
Bethel, W.M. & Holmes, J.C. (1977) Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–115.Google Scholar
Campos, M.Q. & Vargas, M.V. (1977) Biologia de Protospirura muricola Gedoelst, 1916 y Mastophorus muris (Gmelin, 1790) (Nematoda: Spiruridae), en Costa Rica. I. Huespedes intermediarios. Revista de Biologia Tropical 25, 191–207.Google Scholar
Cezilly, F., Gregoire, A. & Bertin, A. (2000) Conflict between co-occurring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625–630.Google Scholar
Crowden, A.E. & Broom, D.M. (1980) Effects of the eye fluke Diplostomum spathaceum on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour 28, 287–294.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, 265–277.Google Scholar
Haine, E.R., Boucansaud, K. & Rigaud, T. (2005) Conflict between parasites with different transmission strategies infecting an amphipod host. Proceedings of the Royal Society Series B 272, 2505–2510.Google Scholar
Hurd, H. & Fogo, S. (1991) Changes induced by Hymenolepis diminuta (Cestoda) in the behaviour of the intermediate host Tenebrio molitor (Coleoptera). Canadian Journal of Zoology 69, 2291–2294.Google Scholar
Jones, M. & Dayan, T. (2000) Foraging behaviour and microhabitat use by spiny mice, Acomys cahirinus and A. russatus, in the presence of Blanford's fox (Vulpes cana) odor. Journal of Chemical Ecology 26, 455–469.Google Scholar
Karvonen, A., Seppala, O. & Valtonen, E.T. (2004) Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129, 473–478.Google Scholar
Klein, S.L. (2005) Parasite manipulation of host behaviour: mechanisms, ecology, and future directions. Behavioural Processes 68, 219–221.Google Scholar
Lafferty, K.D. (1992) Foraging on prey that are modified by parasites. American Naturalist 140, 854–867.CrossRefGoogle Scholar
Lafferty, K.D. (1999) The evolution of trophic transmission. Parasitology Today 15, 111–115.Google Scholar
Libersat, F. & Moore, J. (2000) The parasite Moniliformis moniliformis alters the escape response of its cockroach host Periplaneta americana. Journal of Insect Behaviour 13, 103–110.Google Scholar
Lowrie, F.M., Behnke, J.M. & Barnard, C.J. (2004) Density-dependent effects on the survival and growth of the rodent stomach worm Protospirura muricola in laboratory mice. Journal of Helminthology 78, 121–128.Google Scholar
Marriott, D.R., Collins, M.L., Paris, R.M., Gudgin, D.R., Barnard, C.J., McGregor, P.K., Gilbert, F.S., Hartley, J.C. & Behnke, J.M. (1989) Behavioural modification and increased predation risk of Gammarus pulex infected with Polymorphus minutus. Journal of Biological Education 23, 135–141.Google Scholar
Medoc, V., Rigaud, T., Bollache, L. & Beisel, J.-N. (2009) A manipulative parasite increasing an antipredator response decreases its vulnerability to a non-host predator. Animal Behaviour 77, 1235–1241.CrossRefGoogle Scholar
Milinski, M. (1990) Parasites and host decision-making. pp. 95–116in Barnard, C.J. & Behnke, J.M. (Eds) Parasitism and host behaviour. London, UK, Taylor & Francis.Google Scholar
Moore, J. (1984) Parasites that change the behaviour of their hosts. Scientific American 250, 82–89.Google Scholar
Moore, J. (2002) Parasites and the behaviour of animals. Oxford series in ecology and evolution. New York, USA, Oxford University Press.Google Scholar
Moore, J. & Lasswell, J. (1986) Altered behaviour in isopods (Armadillidium vulgare) infected with the nematode Dispharynx nasuta. Journal of Parasitology 72, 186–189.Google Scholar
Mouritsen, K.N. & Poulin, R. (2003) Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal of Parasitology 33, 1043–1050.Google Scholar
Mukaratirwa, S., Pillay, E. & Munsammy, K. (2010) Experimental infection of selected arthropods with spirurid nematodes Spirocerca lupi Railliet & Henry, 1911 and Gongylonema ingluvicola Molin, 1857. Journal of Helminthology 84, 369–374.Google Scholar
Nickol, B.B. (2005) Parasitic manipulation: should we go anywhere? Behavioural Processes 68, 201–203.Google Scholar
Pearl, R., Park, T. & Miner, J.R. (1941) Experimental studies on the duration of life. XVI. Life tables for the flour beetle Tribolium confusum Duval. American Naturalist 75, 5–19.Google Scholar
Poulin, R. (1994a) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109–S118.Google Scholar
Poulin, R. (1994b) Meta-analysis of parasite-induced behavioural changes. Animal Behaviour 48, 137–146.Google Scholar
Poulin, R. (1995) ‘Adaptive’ change in the behaviour of parasitized animals: a critical review. International Journal of Parasitology 25, 1371–1383.Google Scholar
Poulin, R. (2000) Manipulation of host behaviour by parasites: a weakening paradigm? Proceedings of the Royal Society of London Series B 267, 787–792.Google Scholar
Poulin, R. (2010) Parasite manipulation of host behaviour: an update and frequently asked questions. Advances in the Study of Behavior 41, 151–186.Google Scholar
Poulin, R., Curtis, M.A. & Rau, M.E. (1992) Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepods) and its susceptibility to fish predators. Parasitology 105, 265–271.Google Scholar
Quentin, J.C. (1969) Cycle biologique de Protospirura muricola Gedoelst 1916 (Nematoda; Spiruridae). Annales de Parasitologie 44, 485–504.Google Scholar
Rau, M.E. & Putter, L. (1984) Running responses of Trichinella spiralis-infected CD-1 mice. Parasitology 89, 579–583.Google Scholar
Read, A.F. & Allen, J.E. (2000) The economics of immunity. Science 290, 1104–1105.CrossRefGoogle ScholarPubMed
Rigaud, T. & Haine, E.R. (2005) Conflict between co-occurring parasites as a confounding factor in manipulation studies? Behavioural Processes 68, 259–262.Google Scholar
Rigby, M.C., Hechinger, R.F. & Stevens, L. (2002) Why should parasite resistance be costly? Trends in Parasitology 18, 116–120.Google Scholar
Robb, T. & Reid, M.L. (1996) Parasite-induced changes in the behaviour of cestode-infected beetles: adaptation or simple pathology? Canadian Journal of Zoology 74, 1268–1274.Google Scholar
Rohlf, F.J. & Sokal, R.R. (1995) Statistical tables. 3rd edn.San Francisco, USA, W.H. Freeman.Google Scholar
Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E. & Pell, J.K. (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology 51, 331–357.Google Scholar
Seppälä, O. & Jokela, J. (2008) Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biology Letters 4, 663–666.Google Scholar
Seppälä, O., Karvonene, A. & Valtonen, E.T. (2005) Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behaviour 70, 889–894.Google Scholar
Smales, L.R., Harris, P.D. & Behnke, J.M. (2009) A redescription of Protospirura muricola Gedoelst, 1916 (Nematoda: Spiruridae), a parasite of murid rodents. Systematic Parasitology 72, 15–26.Google Scholar
Sohal, R.S. & Buchan, P.B. (1981) Relationship between physical activity and life span in the adult housefly, Musca domestica. Experimental Gerontology 16, 157–162.Google Scholar
Soliman, M.H. & Lints, F.A. (1975) Longevity, growth rate and related traits among strains of Tribolium castaneum. Gerontologia 21, 102–116.CrossRefGoogle ScholarPubMed
Tain, L., Perrot-Minnot, M.-J. & Cezilly, F. (2006) Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proceedings of the Royal Society of London, Series B 273, 3039–3045.Google Scholar
Tain, L., Perrot-Minnot, M.-J. & Cezilly, F. (2007) Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species. Biology Letters 3, 69–72.Google Scholar
Thomas, F., Poulin, R. & Renaud, F. (1998) Nonmanipulative parasites in manipulated hosts: ‘hitch-hikers’ or simply ‘lucky passengers’? Journal of Parasitology 84, 1059–1061.CrossRefGoogle ScholarPubMed
Thomas, F., Adamo, S. & Moore, J. (2005) Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.Google Scholar
Thomas, F., Poulin, R. & Brodeur, J. (2010) Host manipulation by parasites: a multidimensional phenomenon. Oikos 119, 1217–1223.Google Scholar
Voge, M. & 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, 549–580.Google Scholar
Vyas, A. & Sapolsky, R. (2010) Manipulation of host behaviour by Toxoplasma gondii: what is the minimum a proposed proximate mechanism should explain? Folia Parasitologica 57, 88–94.CrossRefGoogle ScholarPubMed
Webster, J.P., Gowtage-Sequeira, S., Berdoy, M. & Hurd, H. (2000) Predation of beetles (Tenebrio molitor) infected with tapeworms (Hymenolepis diminuta): a note of caution for the Manipulation Hypothesis. Parasitology 120, 313–318.Google Scholar
Worth, A.R., Lymbery, A.J. & Thompson, R.A.C. (2013) Adaptive host manipulation by Toxoplasma gondii: fact or fiction? Trends in Parasitology 29, 150–156.Google Scholar