in

Schistocephalus parasite infection alters sticklebacks’ movement ability and thereby shapes social interactions

  • 1.

    Poulin, R. Evolutionary Ecology of Parasites (Princeton University Press, Princeton, 2011).

    Google Scholar 

  • 2.

    Barber, I., Hoare, D. J. & Krause, J. Effects of parasites on fish behaviour: A review and evolutionary perspective. Rev. Fish Biol. Fish. 10, 131–165 (2000).

    Google Scholar 

  • 3.

    Binning, S. A., Shaw, A. K. & Roche, D. G. Parasites and host performance: Incorporating infection into our understanding of animal movement. Integr. Comp. Biol. 57, 267–280 (2017).

    PubMed  Google Scholar 

  • 4.

    Lafferty, K. D. & Shaw, J. C. Comparing mechanisms of host manipulation across host and parasite taxa. J. Exp. Biol. 216, 56–66 (2012).

    Google Scholar 

  • 5.

    McElroy, E. J. & de Buron, I. Host performance as a target of manipulation by parasites: A meta-analysis. J. Parasitol. 100, 399–410 (2014).

    PubMed  Google Scholar 

  • 6.

    Ward, A. J. W., Hoare, D. J., Couzin, I. D., Broom, M. & Krause, J. The effects of parasitism and body length on positioning within wild fish shoals. J. Anim. Ecol. 71, 10–14 (2002).

    Google Scholar 

  • 7.

    Krause, J. & Godin, J.-G.J. Influence of parasitism on the shoaling behaviour of banded killifish, Fundulus diaphanus. Can. J. Zool. 72, 1775–1779 (1994).

    Google Scholar 

  • 8.

    Barber, I., Huntingford, F. A. & Crompton, D. W. T. The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 132, 1223–1240 (1995).

    Google Scholar 

  • 9.

    Barber, I. & Scharsack, J. P. The three-spined stickleback-Schistocephalus solidus system: An experimental model for investigating host-parasite interactions in fish. Parasitology 137, 411–424 (2010).

    CAS  PubMed  Google Scholar 

  • 10.

    Pennycuick, L. Quantitative effects of 3 species of parasites on a population of three-spined sticklebacks, Gasterosteus aculeatus. J. Zool. 165, 143–162 (1971).

    Google Scholar 

  • 11.

    Barber, I. & Svensson, P. A. Effects of experimental Schistocephalus solidus infections on growth, morphology and sexual development of female three-spined sticklebacks, Gasterosteus aculeatus. Parasitology 126, 359–367 (2003).

    CAS  PubMed  Google Scholar 

  • 12.

    Walkey, M. & Meakins, R. H. An attempt to balance the energy budget of a host-parasite system. J. Fish Biol. 2, 361–372 (1970).

    Google Scholar 

  • 13.

    Lester, R. J. G. The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behavior of the fish. Can. J. Zool. 49, 361–366 (1971).

    ADS  CAS  PubMed  Google Scholar 

  • 14.

    Meakins, R. H. & Walkey, M. The effects of parasitism by the plerocercoid of Schistocephalus solidus Muller 1776 (Pseudophyllidea) on the respiration of the three-spined stickleback Gasterosteus aculeatus L. J. Fish Biol. 7, 817–824 (1975).

    Google Scholar 

  • 15.

    Arme, C. & Owen, R. W. Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Müller, 1776), with special reference to pathological effects. Parasitology 57, 301–314 (1967).

    CAS  PubMed  Google Scholar 

  • 16.

    Barber, I. A non-invasive morphometric technique for estimating cestode plerpcercoid burden in small freshwater fish. J. Fish Biol. 51, 654–658 (1997).

    Google Scholar 

  • 17.

    Dingemanse, N. J., Oosterhof, C., Van Der Plas, F. & Barber, I. Variation in stickleback head morphology associated with parasite infection. Biol. J. Linn. Soc. 96, 759–768 (2009).

    Google Scholar 

  • 18.

    Giles, N. Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus L. Anim. Behav. 31, 1192–1194 (1983).

    Google Scholar 

  • 19.

    Milinski, M. Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93, 203–215 (1985).

    Google Scholar 

  • 20.

    Godin, J.-G.J. & Sproul, C. D. Risk taking in parasitized sticklebacks under threat of predation: Effects of energetic need and food availability. Can. J. Zool. 66, 2360–2367 (1988).

    Google Scholar 

  • 21.

    Grécias, L., Valentin, J. & Aubin-Horth, N. Testing the parasite mass burden effect on alteration of host behaviour in the Schistocephalus–stickleback system. J. Exp. Biol. 221, jeb174748 (2018).

    PubMed  Google Scholar 

  • 22.

    Giles, N. Predation risk and reduced foraging activity in fish: Experiments with parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L. J. Fish Biol. 31, 37–44 (1987).

    Google Scholar 

  • 23.

    Talarico, M. et al. Specific manipulation or systemic impairment? Behavioural changes of three-spined sticklebacks (Gasterosteus aculeatus) infected with the tapeworm Schistocephalus solidus. Behav. Ecol. Sociobiol. 71, 1–10 (2017).

    Google Scholar 

  • 24.

    Pascoe, D. & Mattey, D. Dietary stress in parasitized and non-parasitized Gasterosteus aculeatus L. Zeitschrift für Parasitenkd. 186, 179–186 (1977).

    Google Scholar 

  • 25.

    Ness, J. H. & Foster, S. A. Parasite-associated phenotype modifications in threespine stickleback. Oikos 85, 127–134 (1999).

    Google Scholar 

  • 26.

    Tierney, J. F., Huntingford, F. A. & Crompton, D. W. T. The relationship between infectivity of Schistocephalus solidus (Cestoda) and anti-predator behaviour of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Anim. Behav. 46, 603–605 (1993).

    Google Scholar 

  • 27.

    Barber, I., Walker, P. & Svensson, P. A. Behavioural responses to simulated avian predation in female three-spined sticklebacks: The effect of experimental Schistocephalus solidus infections. Behaviour 141, 1425–1440 (2004).

    Google Scholar 

  • 28.

    Grécias, L., Hébert, F. O., Berger, C. S., Barber, I. & Aubin-Horth, N. Can the behaviour of threespine stickleback parasitized with Schistocephalus solidus be replicated by manipulating host physiology?. J. Exp. Biol. 220, 237–246 (2017).

    PubMed  Google Scholar 

  • 29.

    Peacock, S. D. Some Effects of the Cestode Schistocephalus solidus on the Threespine Stickleback Gasterosteus aculeatus (The University of British Columbia, Vancouver, 1972).

    Google Scholar 

  • 30.

    Blake, R. W., Kwok, P. Y. L. & Chan, K. H. S. Effects of two parasites, Schistocephalus solidus (Cestoda) and Bunodera spp. (Trematoda), on the escape fast-start performance of three-spined sticklebacks. J. Fish Biol. 69, 1345–1355 (2006).

    Google Scholar 

  • 31.

    Hafer, N. & Milinski, M. An experimental conflict of interest between parasites reveals the mechanism of host manipulation. Behav. Ecol. 27, 617–627 (2016).

    PubMed  Google Scholar 

  • 32.

    Jolles, J. W., King, A. J. & Killen, S. S. The role of individual heterogeneity in collective animal behaviour. Trends Ecol. Evol. 35, 278–291 (2020).

    PubMed  Google Scholar 

  • 33.

    Barber, I., Huntingford, F. A. & Crompton, D. W. T. The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish. J. Fish Biol. 47, 524–536 (1995).

    Google Scholar 

  • 34.

    Barber, I. & Huntingford, F. A. Parasite infection alters schooling behaviour: Deviant positioning of helminth-infected minnows in conspecific groups. Proc. R. Soc. B 263, 1095–1102 (1996).

    ADS  Google Scholar 

  • 35.

    Radabauch, D. C. Changes in minnow, Pimephales promelas Rafinesque, schooling behaviour associated with infections of brain-encysted larvae of the fluke, Ornithodiplostomum ptychocheilus. J. Fish Biol. 16, 621–628 (1980).

    Google Scholar 

  • 36.

    Hoare, D. J., Ruxton, G. D., Godin, J. G. J. & Krause, J. The social organization of free-ranging fish shoals. Oikos 89, 546–554 (2000).

    Google Scholar 

  • 37.

    Demandt, N. et al. Parasite-infected sticklebacks increase the risk-taking behaviour of uninfected group members. Proc. R. Soc. B 285, 20180956 (2018).

    PubMed  Google Scholar 

  • 38.

    Ward, A. J. W., Duff, A. J., Krause, J. & Barber, I. Shoaling behaviour of sticklebacks infected with the microsporidian parasite, Glugea anomala. Environ. Biol. Fishes 72, 155–160 (2005).

    Google Scholar 

  • 39.

    Krause, J., Godin, J. J. & Brown, D. Phenotypic variability within and between fish shoals. Ecology 77, 1586–1591 (1996).

    Google Scholar 

  • 40.

    Maximino, C. et al. Measuring anxiety in zebrafish: A critical review. Behav. Brain Res. 214, 157–171 (2010).

    PubMed  Google Scholar 

  • 41.

    Poulin, R. Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions. Advances in the Study of Behavior, Vol. 41, (Elsevier Inc., Amsterdam, 2010).

  • 42.

    Domenici, P. The scaling of locomotor performance in predator-prey encounters: From fish to killer whales. Comp. Biochem. Physiol. Part A 131, 169–182 (2001).

    CAS  Google Scholar 

  • 43.

    Fish, F. E. Swimming strategies for energy economy. In Fish locomotion: An eco-ethological perspective (eds Domenici, P. & Kapoor, B. G.) 90–122 (Science Publishers, 2010).

  • 44.

    Binning, S. A., Roche, D. G. & Layton, C. Ectoparasites increase swimming costs in a coral reef fish. Biol. Lett. 9, 20120927–20120927 (2012).

    Google Scholar 

  • 45.

    Domenici, P. Escape responses in fish: Kinematics, performance and behavior. In Fish locomotion: An eco-ethological perspective (eds Domenici, P. & Kapoor, B. G.) 123–170 (Science Publishers, 2010).

  • 46.

    Jolles, J. W., Boogert, N. J., Sridhar, V. H., Couzin, I. D. & Manica, A. Consistent individual differences drive collective behavior and group functioning of schooling fish. Curr. Biol. 27, 2862–2868 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 47.

    Tunstrøm, K. et al. Collective states, multistability and transitional behavior in schooling fish. PLoS Comput. Biol. 9, e1002915 (2013).

    MathSciNet  PubMed  PubMed Central  Google Scholar 

  • 48.

    Jolles, J. W., Laskowski, K. L., Boogert, N. J. & Manica, A. Repeatable group differences in the collective behaviour of stickleback shoals across ecological contexts. Proc. R. Soc. B 285, 20172629 (2018).

    PubMed  Google Scholar 

  • 49.

    Couzin, I. D., Krause, J., James, R., Ruxton, G. D. & Franks, N. R. Collective memory and spatial sorting in animal groups. J. Theor. Biol. 218, 1–11 (2002).

    MathSciNet  PubMed  Google Scholar 

  • 50.

    Pettit, B., Ákos, Z., Vicsek, T. & Biro, D. Speed determines leadership and leadership determines learning during pigeon flocking. Curr. Biol. 25, 3132–3137 (2015).

    CAS  PubMed  Google Scholar 

  • 51.

    Ioannou, C. C., Guttal, V. & Couzin, I. D. Predatory fish select for coordinated collective motion in virtual prey. Science 337, 1212–1215 (2012).

    ADS  CAS  PubMed  Google Scholar 

  • 52.

    Jones, K. A., Jackson, A. L. & Ruxton, G. D. Prey jitters; Protean behaviour in grouped prey. Behav. Ecol. 22, 831–836 (2011).

    Google Scholar 

  • 53.

    Tierney, J. F. & Crompton, D. W. Infectivity of plerocercoids of Schistocephalus solidus (Cestoda: Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus. J. Parasitol. 78, 1049–1054 (1992).

    CAS  PubMed  Google Scholar 

  • 54.

    Berger, C. S. & Aubin-Horth, N. The secretome of a parasite alters its host’s behaviour but does not recapitulate the behavioural response to infection. Proc. R. Soc. B 287, 20200412 (2020).

    PubMed  Google Scholar 

  • 55.

    Franke, F., Armitage, S. A. O., Kutzer, M. A. M., Kurtz, J. & Scharsack, J. P. Environmental temperature variation influences fitness trade-offs and tolerance in a fish-tapeworm association. Parasites Vectors 10, 1–11 (2017).

    Google Scholar 

  • 56.

    Hopkins, B. Y. C. A. & Smyth, J. D. Notes on the morphology and life history of Schistocehpaus solidus (Cestoda: Diphyllobothriidae. Parasitology 41, 283–291 (1951).

    CAS  PubMed  Google Scholar 

  • 57.

    Huntingford, F. A. & Ruiz-Gomez, M. L. Three-spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology. J. Fish Biol. 75, 1943–1976 (2009).

    CAS  PubMed  Google Scholar 

  • 58.

    Webster, M. M. & Laland, K. N. Evaluation of a non-invasive tagging system for laboratory studies using three-spined sticklebacks Gasterosteus aculeatus. J. Fish Biol. 75, 1868–1873 (2009).

    CAS  PubMed  Google Scholar 

  • 59.

    Jolles, J. W., Aaron Taylor, B. & Manica, A. Recent social conditions affect boldness repeatability in individual sticklebacks. Anim. Behav. 112, 139–145 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 60.

    Jolles, J. W. Pirecorder: Controlled and automated image and video recording with the raspberry pi. (2019). https://doi.org/10.5281/zenodo.2529515

  • 61.

    Krause, J., Reeves, P. & Hoare, D. J. Positioning behaviour in Roach shoals: The role of body length and nutritional state. Behaviour 135, 1031–1039 (1998).

    Google Scholar 

  • 62.

    Katz, Y., Tunstrøm, K., Ioannou, C. C., Huepe, C. & Couzin, I. D. Inferring the structure and dynamics of interactions in schooling fish. Proc. Natl. Acad. Sci. 108, 18720–18725 (2011).

    ADS  CAS  PubMed  Google Scholar 


  • Source: Ecology - nature.com

    Impact of 10-Myr scale monsoon dynamics on Mesozoic climate and ecosystems

    Growth dynamics of galls and chemical defence response of Pinus thunbergii Parl. to the pine needle gall midge, Thecodiplosis japonensis Uchida & Inouye (Diptera: Cecidomyiidae)