Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T22:30:03.845Z Has data issue: false hasContentIssue false
  • English
  • Français

The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish

Published online by Cambridge University Press:  16 October 2009

I. BARBER  and
J. P. SCHARSACK
I. BARBER*
Affiliation:
Department of Biology, University of Leicester, University Road, LeicesterLE1 7RH, UK
J. P. SCHARSACK
Affiliation:
Animal Evolutionary Ecology Group, Institute for Evolution and Biodiversity, University of Münster, Huefferstr. 1, D-48149Münster, GERMANY
*
*Corresponding author: Tel: +44(0)116 252 3462. Fax: +44(0)116 252 3330. E-mail: ib50@le.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Plerocercoids of the pseudophyllidean cestode Schistocephalus solidus infect the three-spined stickleback Gasterosteus aculeatus, with important consequences for the biology of host fish. Techniques for culturing the parasite in vitro and generating infective stages that can be used to infect sticklebacks experimentally have been developed, and the system is increasingly used as a laboratory model for investigating aspects of host-parasite interactions. Recent experimental laboratory studies have focused on the immune responses of hosts to infection, the consequences of infection for the growth and reproductive development of host fish and the effects of infection on host behaviour. Here we introduce the host and the parasite, review the major findings of these recent experimental infection studies and identify further aspects of host parasite interactions that might be investigated using the system.

Keywords

Three-spined sticklebackGasterosteus aculeatusCestodaPseudophyllidealaboratory modelgrowthimmunologyLigula intestinalisbehaviourfitness
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 411 - 424
Copyright
Copyright © Cambridge University Press 2009

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

REFERENCES

Adamo, S. A. (2002). Modulating the modulators: parasites, neuromodulators and host behavioural change. Brain, Behavior and Evolution 60, 370–377.Google Scholar
Aeschlimann, P., Häberli, M. and Milinski, M. (2000). Threat-sensitive feeding strategy of immature sticklebacks (Gasterosteus aculeatus) in response to recent experimental infection with the cestode Schistocephalus solidus. Behavioral Ecology and Sociobiology 49, 1–7.CrossRefGoogle Scholar
Andersson, M. (1994). Sexual Selection, Princeton University Press, Princeton.CrossRefGoogle Scholar
Arme, C. and Owen, R. W. (1967). Infections of 3-spined stickleback Gasterosteus aculeatus L with plerocercoid larvae of Schistocephalus solidus (Müller 1776) with special reference to pathological effects. Parasitology 57, 301–304.CrossRefGoogle Scholar
Arnott, S. A., Barber, I. and Huntingford, F. A. (2000). Parasite-associated growth enhancement in a fish-cestode system. Proceedings of the Royal Society of London Series B-Biological Sciences 267, 657–663.CrossRefGoogle Scholar
Bagamian, K. H., Heins, D. C. and Baker, J. A. (2004). Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. Journal of Fish Biology 64, 1568–1576.CrossRefGoogle Scholar
Bakker, T. C. M. and Milinski, M. (1991). The advantages of being red – sexual selection in the stickleback. In Conference on Behavioural Ecology of Fishes, pp. 287–300. Erice, Italy.Google Scholar
Barber, I. (1997). A non-invasive morphometric technique for estimating cestode plerocercoid burden in small freshwater fish. Journal of Fish Biology 51, 654–658.CrossRefGoogle Scholar
Barber, I. (2005). Parasites grow larger in faster growing fish hosts. International Journal for Parasitology 35, 137–143.Google Scholar
Barber, I. (2007). Host–parasite interactions of the three-spined stickleback. In Biology of the Three-Spined Stickleback (eds. Östlund-Nilsson, S., Mayer, I. and Huntingford, F. A.), pp. 271–318. CRC Press, Boca Raton, FL.Google Scholar
Barber, I. and Arnott, S. A. (2000). Split-clutch IVF: A technique to examine indirect fitness consequences of mate preferences in sticklebacks. Behaviour 137, 1129–1140.CrossRefGoogle Scholar
Barber, I., Arnott, S. A., Braithwaite, V. A., Andrew, J. and Huntingford, F. A. (2001). Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proceedings of the Royal Society of London Series B-Biological Sciences 268, 71–76.CrossRefGoogle ScholarPubMed
Barber, I., Downey, L. C. and Braithwaite, V. A. (1998). Parasitism, oddity and the mechanism of shoal choice. Journal of Fish Biology 53, 1365–1368.CrossRefGoogle Scholar
Barber, I. and Huntingford, F. A. (1995). The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 132, 1223–1240.Google Scholar
Barber, I., Huntingford, F. A. and Crompton, D. W. T. (1995). The effect of hunger and cestode parasitism on the shoaling decisions of small fresh-water fish. Journal of Fish Biology 47, 524–536.CrossRefGoogle Scholar
Barber, I. and Ruxton, G. D. (1998). Temporal prey distribution affects the competitive ability of parasitized sticklebacks. Animal Behaviour 56, 1477–1483.Google Scholar
Barber, I. and Svensson, P. A. (2003). Effects of experimental Schistocephalus solidus infections on growth, morphology and sexual development of female three-spined sticklebacks, Gasterosteus aculeatus. Parasitology 126, 359–367.CrossRefGoogle ScholarPubMed
Barber, I., Walker, P. and Svensson, P. A. (2004). Behavioural responses to simulated avian predation in female three spined sticklebacks: The effect of experimental Schistocephalus solidus infections. Behaviour 141, 1425–1440.CrossRefGoogle Scholar
Barber, I., Wright, H., Arnott, S. and Wootton, R. (2008). Growth and energetics in the stickleback–Schistocephalus host–parasite system: a review of experimental infection studies. Behaviour 145, 647–668.Google Scholar
Bell, A. M. (2005). Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). Journal of Evolutionary Biology 18, 464–473.CrossRefGoogle ScholarPubMed
Bell, A. M. and Stamps, J. A. (2004). Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus. Animal Behaviour 68, 1339–1348.CrossRefGoogle Scholar
Bell, M. A. and Foster, S. A. (Eds.) (1994). The Evolutionary Biology of the Threespine Stickleback, Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Bergersen, R. (1996). Sticklebacks from Greenland. Journal of Fish Biology 48, 799–801.CrossRefGoogle Scholar
Bråten, T. (1966). Host specificity in Schistocephalus solidus. Parasitology 56, 657–664.CrossRefGoogle ScholarPubMed
Bunnajirakul, S., Steinhagen, D., Hetzel, U., Korting, W. and Drommer, W. (2000). A study of sequential histopathology of Trypanoplasma borreli (Protozoa: Kinetoplastida) in susceptible common carp Cyprinus carpio. Diseases of Aquatic Organisms 39, 221–229.CrossRefGoogle ScholarPubMed
Candolin, U. and Voigt, H. R. (2001). No effect of a parasite on reproduction in stickleback males: a laboratory artefact? Parasitology 122, 457–464.Google Scholar
Chappell, L. H. (1969). Parasites of three-spined stickleback Gasterosteus aculeatus L from a Yorkshire Pond. 1. Seasonal variation of parasite fauna. Journal of Fish Biology 1, 137–152.CrossRefGoogle Scholar
Chubb, J. C., Seppala, O., Luscher, A., Milinski, M. and Valtonen, E. T. (2006). Schistocephalus cotti n. sp (Cestoda: Pseudophyllidea) plerocercoids from bullheads Cottus gobio L. in an Arctic river in Finland, with a key to the plerocercoids of the Palaearctic species of the genus. Systematic Parasitology 65, 161–170.CrossRefGoogle Scholar
Clarke, A. S. (1954). Studies on the life cycle of the pseudophyllidean cestode Schistocephalus solidus. Proceedings of the Zoological Society of London 124, 257–302.CrossRefGoogle Scholar
Colosimo, P. F., Hosemann, K. E., Balabhadra, S., Villarreal, G., Dickson, M., Grimwood, J., Schmutz, J., Myers, R. M., Schluter, D. and Kingsley, D. M. (2005). Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307, 1928–1933.CrossRefGoogle ScholarPubMed
Coombs, I. and Crompton, D. W. T. (1991). A Guide to Human Helminths. Taylor & Francis Ltd, London.Google Scholar
Dantzer, R. (2004). Cytokine-induced sickness behaviour: A neuroimmune response to activation of innate immunity. European Journal of Pharmacology 500, 399–411.CrossRefGoogle ScholarPubMed
Dick, T. L. (1816). Account of the worm with which the stickleback is infested. Annals of Philosophy 7, 106–109.Google Scholar
Dörücü, M., Wilson, D. and Barber, I. (2007). Differences in adult egg output of Schistocephalus solidus from singly- and multiply-infected sticklebacks. Journal of Parasitology 93, 1521–1523.CrossRefGoogle ScholarPubMed
Engelsma, M. Y., Huising, M. O., Van Muiswinkel, W. B., Flik, G., Kwang, J., Savelkoul, H. F. and Verburg-Van Kemenade, B. M. (2002). Neuroendocrine-immune interactions in fish: a role for interleukin-1. Veterinary Immunology and Immunopathology 87, 467–479.Google Scholar
Folstad, I., Hope, A. M., Karter, A. and Skorping, A. (1994). Sexually selected color in male sticklebacks – a signal of both parasite exposure and parasite resistance. Oikos 69, 511–515.Google Scholar
French, J. R. P. and Muzzall, P. M. (2008). First report of Schistocephalus sp (Cestoda: Pseudophyllidea) in slimy sculpin, Cottus cognatus Richardson, 1836, from Lake Michigan, USA. Comparative Parasitology 75, 132–134.CrossRefGoogle Scholar
Gibson, G. (2005). The synthesis and evolution of a supermodel. Science 307, 1890–1891.CrossRefGoogle ScholarPubMed
Giles, N. (1983). Behavioral effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the 3-spined stickleback, Gasterosteus aculeatus L. Animal Behaviour 31, 1192–1194.Google Scholar
Giles, N. (1987 a). A comparison of the behavioral responses of parasitized and non-parasitized 3-spined sticklebacks, Gasterosteus aculeatus L, to progressive hypoxia. Journal of Fish Biology 30, 631–638.CrossRefGoogle Scholar
Giles, N. (1987 b). Predation risk and reduced foraging activity in fish – Experiments with parasitized and non-parasitized 3-spined sticklebacks, Gasterosteus aculeatus L. Journal of Fish Biology 31, 37–44.Google Scholar
Godin, J. G. J. and Sproul, C. D. (1988). Risk-taking in parasitized sticklebacks under threat of predation – Effects of energetic need and food availability. Canadian Journal of Zoology-Revue Canadienne De Zoologie 66, 2360–2367.Google Scholar
Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J. C. and Parker, G. A. (2009). When to go: optimization of host switching in parasites with complex life cycles. Evolution 63, 1976–1986.Google Scholar
Hammerschmidt, K. and Kurtz, J. (2005). Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: Individual variation and fitness consequences. International Journal for Parasitology 35, 1499–1507.CrossRefGoogle ScholarPubMed
Hammerschmidt, K. and Kurtz, J. (2007). Schistocephalus solidus: Establishment of tapeworms in sticklebacks – fast food or fast lane? Experimental Parasitology 116, 142–149.Google Scholar
Hammerschmidt, K. and Kurtz, J. (2009). Ecological immunology of a tapeworms' interaction with its two consecutive hosts. Advances in Parasitology 68, 111–137.CrossRefGoogle ScholarPubMed
Hart, B. L. (1990). Behavioral adaptations to pathogens and parasites – 5 strategies. Neuroscience and Biobehavioral Reviews 14, 273–294.CrossRefGoogle ScholarPubMed
Hart, B. L. (1992). Behavioral adaptations to parasites – an ethological approach. Journal of Parasitology 78, 256–265.Google Scholar
Hart, B. L. (1997). Behavoural defence. In Host-Parasite Evolution: General Principle and Avian Models (eds. Clayton, D. H. & Moore, J.), pp. 59–77. Oxford University Press, Oxford, UK.Google Scholar
Heins, D. C. and Baker, J. A. (2008). The stickleback-Schistocephalus host-parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145, 625–645.Google Scholar
Heins, D. C., Singer, S. S. and Baker, J. A. (1999). Virulence of the cestode Schistocephalus solidus and reproduction in infected threespine stickleback, Gasterosteus aculeatus. Canadian Journal of Zoology-Revue Canadienne De Zoologie 77, 1967–1974.Google Scholar
Herve, M., Angeli, V., Pinzar, E., Wintjens, R., Faveeuw, C., Narumiya, S., Capron, A., Urade, Y., Capron, M., Riveau, G. and Trottein, F. (2003). Pivotal roles of the parasite PGD(2) synthase and of the host D prostanoid receptor 1 in schistosome immune evasion. European Journal of Immunology 33, 2764–2772.Google Scholar
Hoberg, E. P., Henny, C. J., Hedstrom, O. R. and Grove, R. A. (1997). Intestinal helminths of river otters (Lutra canadensis) from the Pacific Northwest. Journal of Parasitology 83, 105–110.CrossRefGoogle ScholarPubMed
Hopkins, C. A. and Smyth, J. D. (1951). Notes on the morphology and life history of Schistocephalus solidus (Cestoda, Diphyllobothriidae). Parasitology 41, 283–291.Google Scholar
Hyslop, E. J. and Chubb, J. C. (1983). Schistocephalus pungitii Dubinina, 1959 (Cestoda) in Britain. Parasitology 87, R30–R30.Google Scholar
Jäger, I. and Schjørring, S. (2006). Multiple infections: Relatedness and time between infections affect the establishment and growth of the cestode Schistocephalus solidus in its stickleback host. Evolution 60, 616–622.Google ScholarPubMed
Jakobsen, P. J., Johnsen, G. H. and Larsson, P. (1988). Effects of predation risk and parasitism on the feeding ecology, habitat use, and abundance of lacustrine threespine stickleback (Gasterosteus aculeatus). Canadian Journal of Fisheries and Aquatic Sciences 45, 426–431.CrossRefGoogle Scholar
Jakobsen, P. J. and Wedekind, C. (1998). Copepod reaction to odor stimuli influenced by cestode infection. Behavioral Ecology 9, 414–418.CrossRefGoogle Scholar
Kennedy, C. R. (1974). Checklist of British and Irish freshwater fish parasites with notes on their distribution. Journal of Fish Biology 6, 613–644.Google Scholar
Keymer, A. E. and Read, A. F. (1991). Behavioural ecology: the impact of parasitism. In Parasite–Host Associations, Coexistence or Conflict (eds. Toft, C. A., Aeschlimann, A. and Bolis, L.), Oxford Scientific Publications, Oxford, UK.Google Scholar
Kingsley, D. M. (2003). Sequencing the genome of threespine sticklebacks (Gasterosteus aculeatus). In National Human Genome Research Institute White Paper http://www.genome.gov/Pages/Research/Sequencing/SeqProposals/SticklebackSEQ.pdfGoogle Scholar
Kingsley, D. M., Zhu, B. L., Osoegawa, K., De Jong, P. J., Schein, J., Marra, M., Peichel, C., Amamiya, C., Schluter, D., Balabhadra, S., Friedlander, B., Cha, Y. M., Dickson, M., Grimwood, J., Schmutz, J., Talbot, W. S. and Myers, R. (2004). New genomic tools for molecular studies of evolutionary change in threespine sticklebacks. Behaviour 141, 1331–1344.Google Scholar
Kurtz, J., Kalbe, M., Aeschlimann, P. B., Haberli, M. A., Wegner, K. M., Reusch, T. B. H. and Milinski, M. (2004). Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proceedings of the Royal Society of London Series B-Biological Sciences 271, 197–204.Google Scholar
Lafferty, K. D. (1992). Foraging on prey that are modified by parasites. American Naturalist 140, 854–867.CrossRefGoogle Scholar
Lester, R. J. G. (1971). Influence of Schistocephalus plerocercoids on respiration of Gasterosteus and a possible resulting effect on behavior of fish. Canadian Journal of Zoology 49, 361–366.Google Scholar
Lobue, C. P. and Bell, M. A. (1993). Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the threespine stickleback. American Naturalist 142, 725–735.Google Scholar
Loot, G., Giraudel, J. L. and Lek, S. (2002). A non-destructive morphometric technique to predict Ligula intestinalis L. plerocercoid load in roach (Rutilus rutilus L.) abdominal cavity. Ecological Modelling 156, 1–11.Google Scholar
Lüscher, A. and Wedekind, C. (2002). Size-dependent discrimination of mating partners in the simultaneous hermaphroditic cestode Schistocephalus solidus. Behavioral Ecology 13, 254–259.Google Scholar
MacColl, A. D. C. (2009). Parasite burdens differ between sympatric three-spined stickleback species. Ecography 32, 153–160.CrossRefGoogle Scholar
MacNab, V. L., Katsiadaki, I. and Barber, I. (in press). Reproductive potential of Schistocephalus solidus infected male three-spined stickleback (Gasterosteus aculeatus) from two UK populations. Journal of Fish Biology in press.Google Scholar
Maizels, R. M. and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733–744.Google Scholar
Manning, M. J. (1994). Fishes. In Immunology: A Comparative Approach (ed. Turner, R. J.), John Willey & Sons, Chichester, New York, USA.Google Scholar
McKinnon, J. S., Mori, S., Blackman, B. K., David, L., Kingsley, D. M., Jamieson, L., Chou, J. and Schluter, D. (2004). Evidence for ecology's role in speciation. Nature 429, 294–298.Google Scholar
McPhail, J. D. and Peacock, S. D. (1983). Some effects of the cestode (Schistocephalus solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus): Evolutionary aspects of a host-parasite interaction. Canadian Journal of Zoology-Revue Canadienne De Zoologie 61, 901–908.Google Scholar
Milinski, M. (1984). Parasites determine a predator's optimal feeding strategy. Behavioral Ecology and Sociobiology 15, 35–37.CrossRefGoogle Scholar
Milinski, M. (1985). Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L) under competition for food. Behaviour 93, 203–215.Google Scholar
Milinski, M. (1990). Parasites and host decision-making. In Parasitism and Host Behaviour (eds. Barnard, C. J. and Behnke, J. M.), pp. 95–116. Taylor and Francis, London.Google Scholar
Milinski, M. and Bakker, T. C. M. (1990). Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344, 330–333.CrossRefGoogle Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–216.CrossRefGoogle Scholar
Ness, J. H. and Foster, S. A. (1999). Parasite-associated phenotype modifications in threespine stickleback. Oikos 85, 127–134.CrossRefGoogle Scholar
Orr, T. S. C., Hopkins, C. A. and Charles, G. H. (1969). Host specificity and rejection of Schistocephalus solidus. Parasitology 59, 683–690.CrossRefGoogle Scholar
Östlund-Nilsson, S., Mayer, I. and Huntingford, F. A. (2006). Biology of the Three-Spined Stickleback, CRC Press, Boca Raton. FL.Google Scholar
Øverli, O., Páll, M., Borg, B., Jobling, M. and Winberg, S. (2001). Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. Proceedings of the Royal Society of London Series B-Biological Sciences 268, 1411–1415.CrossRefGoogle ScholarPubMed
Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K. and Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution 63, 448–458.CrossRefGoogle ScholarPubMed
Pasternak, A. F., Huntingford, F. A. and Crompton, D. W. T. (1995). Changes in metabolism and behaviour of the fresh-water copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 110, 395–399.Google Scholar
Peichel, C. L., Nereng, K. S., Ohgi, K. A., Cole, B. L. E., Colosimo, P. F., Buerkle, C. A., Schluter, D. and Kingsley, D. M. (2001). The genetic architecture of divergence between threespine stickleback species. Nature 414, 901–905.CrossRefGoogle ScholarPubMed
Pennycuick, L. (1971). Quantitative effects of three species of parasites on a population of three-spined sticklebacks, Gasterosteus aculeatus. Journal of Zoology 165, 143–162.CrossRefGoogle Scholar
Poulin, R. (1994). The evolution of parasite manipulation of host behavior – a theoretical analysis. Parasitology 109, S109–S118.Google Scholar
Ranta, E. (1995). Schistocephalus infestation improves prey-size selection by 3-spined sticklebacks, Gasterosteus aculeatus. Journal of Fish Biology 46, 156–158.Google Scholar
Reimchen, T. E. (1997). Parasitism of asymmetrical pelvic phenotypes in stickleback. Canadian Journal of Zoology-Revue Canadienne De Zoologie 75, 2084–2094.Google Scholar
Reimchen, T. E. and Nosil, P. (2001). Lateral plate asymmetry, diet and parasitism in threespine stickleback. Journal of Evolutionary Biology 14, 632–645.CrossRefGoogle Scholar
Rijkers, G. T., Frederixwolters, E. M. H. and Vanmuiswinkel, W. B. (1980). The immune system of cyprinid fish – kinetics and temperature dependence of antibody producing cells in carp (Cyprinus carpio). Immunology 41, 91–97.Google Scholar
Rushbrook, B. J. and Barber, I. (2006). Nesting, courtship and kidney hypertrophy in Schistocephalus-infected male three-spined stickleback from an upland lake. Journal of Fish Biology 69, 870–882.Google Scholar
Scharsack, J. P., Kalbe, M., Derner, R., Kurtz, J. and Milinski, M. (2004). Modulation of granulocyte responses in three-spined sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus. Diseases of Aquatic Organisms 59, 141–150.CrossRefGoogle ScholarPubMed
Scharsack, J. P., Koch, K. and Hammerschmidt, K. (2007). Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proceedings of the Royal Society B-Biological Sciences 274, 3151–3158.Google Scholar
Seppala, T., Chubb, J. C., Niemela, E. and Valtonen, E. T. (2007). Introduced bullheads Cottus gobio and infection with plerocercoids of Schistocephalus cotti in the Utsjoki, an Arctic river in Finland. Journal of Fish Biology 70, 1865–1876.Google Scholar
Shapiro, M. D., Bell, M. A. and Kingsley, D. M. (2006). Parallel genetic origins of pelvic reduction in vertebrates. Proceedings of the National Academy of Sciences, USA 103, 13753–13758.Google Scholar
Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jonsson, B., Schluter, D. and Kingsley, D. M. (2004). Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717–723.Google Scholar
Smyth, J. D. (1946). Studies on tapeworm physiology. I. The cultivation of Schistocephalus solidus in vitro. Journal of Experimental Biology 23, 47–70.Google Scholar
Smyth, J. D. (1947). The physiology of tapeworms. Biological Reviews 22, 214–238.Google Scholar
Smyth, J. D. (1990). In Vitro Cultivation of Parasitic Helminths. CRC Press, Boca Raton, FL.Google Scholar
Smyth, J. D. and Mcmanus, D. P. (1989). The Physiology and Biochemisty of Cestodes, Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Takizawa, F., Araki, K., Kobayashi, I., Moritomo, T., Ototake, M. and Nakanishi, T. (2008 a). Molecular cloning and expression analysis of T-bet in ginbuna crucian carp (Carassius auratus langsdorfii). Molecular Immunology 45, 127–136.Google Scholar
Takizawa, F., Mizunaga, Y., Araki, K., Moritomo, T., Ototake, M. and Nakanishi, T. (2008 b). GATA3 mRNA in ginbuna crucian carp (Carassius auratus langsdorfii): cDNA cloning, splice variants and expression analysis. Developmental and Comparative Immunology 32, 898–907.Google Scholar
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.Google Scholar
Tierney, J. F. (1994). Effects of Schistocephalus solidus (Cestoda) on the food intake and diet of the three-spined stickleback, Gasterosteus aculeatus. Journal of Fish Biology 44, 731–735.Google Scholar
Tierney, J. F. and Crompton, D. W. T. (1992). Infectivity of plerocercoids of Schistocephalus solidus (Cestoda, Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus. Journal of Parasitology 78, 1049–1054.CrossRefGoogle Scholar
Tierney, J. F., Huntingford, F. A. and Crompton, D. W. T. (1993). The relationship between infectivity of Schistocephalus solidus (Cestoda) and antipredator behavior of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour 46, 603–605.Google Scholar
Tierney, J. F., Huntingford, F. A. and Crompton, D. W. T. (1996). Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection. Journal of Fish Biology 49, 483–493.Google Scholar
Urdal, K., Tierney, J. F. and Jakobsen, P. J. (1995). The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. Journal of Parasitology 81, 330–333.CrossRefGoogle Scholar
Vanmuiswinkel, W. B. (1995). The piscine immune system: innate and acquired immunity. In Fish Diseases and Disorders. Volume 1, Protozoan and Metazoan Infections (ed. Woo, P. T. K.), pp. 729–750. CAB International, Wallingford, UK.Google Scholar
Vollmer-Conna, U. (2001). Acute sickness behaviour: an immune system-to-brain communication? Psychological Medicine 31, 761–767.Google Scholar
Walkey, M. and Meakins, R. H. (1970). An attempt to balance energy budget of a host-parasite system. Journal of Fish Biology 2, 361–372.Google Scholar
Wang, L. J., Cao, Y. and Shi, H. N. (2008). Helminth infections and intestinal inflammation. World Journal of Gastroenterology 14, 5125–5132.Google Scholar
Wedekind, C. (1997). The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus. Parasitology 115, 317–324.Google Scholar
Wedekind, C. and Little, T. J. (2004). The clearance of hidden cestode infection triggered by an independent activation of host defense in a teleost fish. Journal of Parasitology 90, 1329–1331.CrossRefGoogle Scholar
Wedekind, C. and Milinski, M. (1996). Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus? An experimental analysis of behavioural resistance. Parasitology 112, 371–383.Google Scholar
Wegner, K. M., Kalbe, M., Kurtz, J., Reusch, T. B. H. and Milinski, M. (2003). Parasite selection for immunogenetic optimality. Science 301, 1343–1343.CrossRefGoogle ScholarPubMed
Wootton, R. J. (1976). The Biology of the Sticklebacks. Academic Press, London.Google Scholar
Wootton, R. J. (1984). A Functional Biology of Sticklebacks. University of California Press, Berkeley, CA.Google Scholar
Wright, H. A., Wootton, R. J. and Barber, I. (2006). The effect of Schistocephalus solidus infection on meal size of three-spined stickleback. Journal of Fish Biology 68, 801–809.Google Scholar
Wright, H. A., Wootton, R. J. and Barber, I. (2007). Compensatory growth in threespine sticklebacks (Gasterosteus aculeatus) inhibited by experimental Schistocephalus infection. Canadian Journal of Fisheries and Aquatic Sciences 64, 819–826.CrossRefGoogle Scholar