Journal of Ichthyology

, Volume 46, Supplement 2, pp S173–S179

Defense behavior of fish against predators and parasites

  • V. N. Mikheev
  • A. F. Pasternak


This paper is a review of empirical and theoretical studies of the behavioral mechanisms and ecological consequences of the anti-predator and anti-parasite activities of teleost fishes. While the individual and cooperative behaviors used by fish to protect themselves from predators have received marked attention from researchers in the fields of ecology, ethology and applied fish biology, the behaviors by which fish protect themselves from parasites have been poorly investigated. Generally, free-swimming parasites, which are difficult to distinguish, do not elicit any marked behavioral response from fish prior to contact. We hypothesize that the behaviors by which fish avoid parasites are much more efficient for fish in groups than they are for solitary fish. Early avoidance of predators and parasites is compared with the behavioral tactics fish use when such enemies are in close proximity. Individual versus cooperative tactics, as well as the role of learning, are also analyzed. Learning is more important for behaviors which protect fish from predators than those which they use against parasites, especially at the level of individual fish. Finally, we briefly discuss the importance of coordination of anti-predator and anti-parasite activities, which present the most complicated tasks for fish and intriguing problems for researchers.


  1. 1.
    M. O. Afonina and V. N. Mikheev, “Modification of Foraging Behavior of Guppy Poecilia reticulata by Chemical Signals of Cichlids: The Role of Preliminary Acquaintance with the Predator,” J. Ichthyol. 44(Suppl. 2), 175–180 (2004).Google Scholar
  2. 2.
    M. O. Afonina, V. N. Mikheev, and D. S. Pavlov, “Effect of Heterogeneity of the Visual Habitat on Learning a Food Patch Task by the Convict Cichlid Cichlasoma nigrofasciatum (Pisces: Cichlidae),” Dokl. Biol. Sci. 372, 300–302 (2000).PubMedGoogle Scholar
  3. 3.
    R. D. Alexander, “The Evolution of Social Behavior,” Ann. Rev. Ecol. Syst. 5, 325–383 (1974).CrossRefGoogle Scholar
  4. 4.
    R. L. Baker and B. P. Smith, “Conflict between Antipredator and Antiparasite Behaviour in Larval Damselflies,” Oecologia 109, 622–628 (1997).CrossRefGoogle Scholar
  5. 5.
    M. Begon, J. L. Harper, and C. R. Townsend, Ecology. Individuals, Populations and Communities (Blackwell Scientific Publications, Oxford, 1986).Google Scholar
  6. 6.
    D. P. Chivers, G. E. Brown, and R. J. F. Smith, “Familiarity and Shoal Cohesion in Fathead Minnow (Pimephales promelas): Implications for Antipredator Behaviour,” Can. J. Zool. 73, 955–960 (1995).Google Scholar
  7. 7.
    D. Coates, “The Discrimination and Reactions towards Predatory and Non-Predatory Species of Fish by Humbug Damselfish, Dascyllus aruanus (Pisces, Pomacentridae),” Z. Tierpsychol. 52, 347–354 (1980).Google Scholar
  8. 8.
    I. M. Cote and R. Poulin, “Parasitism and Group Size in Social Animals: A Meta-Analysis,” Behav. Ecol. 6, 159–165 (1995).Google Scholar
  9. 9.
    E. Curio, The Ethology of Predation (Springer, Berlin, 1976).Google Scholar
  10. 10.
    E. M. DeBlois, and G. A. Rose, “Cross-Shoal Variability in the Feeding Habits of Migrating Atlantic Cod (Gadus morhua),” Oecologia 108, 192–196 (1996).CrossRefGoogle Scholar
  11. 11.
    M. Edmunds, Defence in Animals (Longman, New York, 1974).Google Scholar
  12. 12.
    J. A. Endler, “Defense against Predators,” in Predator-Prey Relationships, Ed. by M.E. Feder and G.V. Lauder (University of Chicago, Chicago, 1986), pp. 109–134.Google Scholar
  13. 13.
    J. A. Endler, “Interactions between Predators and Prey,” in Behavioural Ecology: An Evolutionary Approach, 3rd ed., Ed. by J.R. Krebs and N.B. Davies (Blackwell Scientific Publ., Oxford, 1991), pp. 169–196.Google Scholar
  14. 14.
    D. F. Frazer, J. F. Gilliam, M. J. Daley, A. N. Le, and G. T. Skalsk, “Explaining Leptokurtic Movement Distributions: Intrapopulation Variation in Boldness and Exploration,” Am. Nat. 158, 124–135 (2001).CrossRefGoogle Scholar
  15. 15.
    L.A. Fuiman and A.E. Magurran, “Development of Predator Defenses in Fishes,” Rev. Fish Biol. Fish. 4, 145–183 (1994).CrossRefGoogle Scholar
  16. 16.
    J.-G. J. Godin, “Antipredator Function of Shoaling in Teleost Fishes: A Selective Review,” Nat. Can. 113, 241–250 (1986).Google Scholar
  17. 17.
    V. Gotceitas and J.-G. J. Godin, “Foraging under the Risk of Predation in Juvenile Atlantic Salmon (Salmo salar L.): Effects of Social Status and Hunger,” Behav. Ecol. Sociobiol. 29, 255–261 (1991).CrossRefGoogle Scholar
  18. 18.
    J. W. A. Grant, “Whether or not to Defend? The Influence of Resource Distribution,” Mar. Behav. Physiol. 23, 137–153 (1993).Google Scholar
  19. 19.
    J. W. A. Grant, “Territoriality,” in Behavioural Ecology of Teleost Fishes, Ed. by J.-G.J. Godin (Oxford University Press, Oxford, 1997), pp. 81–103.Google Scholar
  20. 20.
    M. C. Hager and G. S. Helfman, “Safety in Numbers: Shoal Size Choice by Minnows under Predation Threat,” Behav. Ecol. Sociobiol. 29, 271–276 (1991).CrossRefGoogle Scholar
  21. 21.
    W. D. Hamilton, “Geometry for the Selfish Herd,” J. Theor. Biol. 31, 295–311 (1971).PubMedCrossRefGoogle Scholar
  22. 22.
    L. A. Hawkins, J. D. Armstrong, and A. E. Magurran, “Predator-Induced Hyperventilation in Wild and Hatchery Atlantic Salmon Fry,” J. Fish Biol. 65(Suppl. A), 88–100 (2004).CrossRefGoogle Scholar
  23. 23.
    J. C. Holmes and S. Zohar, “Pathology and Host Behaviour,” in Parasitism and Host Behaviour, Ed. by C.J. Barnard and J.M. Behnke (Taylor and Francis, London, 1990), pp. 34–63.Google Scholar
  24. 24.
    I. Karplus and D. Algom, “Visual Cues for Predator Face Recognition by Reef Fishes,” Z. Tierpsychol. 552, 343–364 (1981).Google Scholar
  25. 25.
    A. Karvonen, O. Seppala and E. T. Valtonen, “Parasite Resistance and Avoidance Behavior in Preventing Eye Fluke Infections in Fish,” Parasitology 129, 159–164 (2004).PubMedCrossRefGoogle Scholar
  26. 26.
    M. H. A. Keenleyside, Diversity and Adaptation in Fish Behaviour (Springer, Berlin, 1979).Google Scholar
  27. 27.
    J. Klein, Immunology (Oxford University Press, Oxford, 1990).Google Scholar
  28. 28.
    J. Krause, “The Effect of ’schreckstoff’ on the Shoaling Behaviour of a Minnow: A Test of Hamilton’s Selfish Herd Theory,” Anim. Behav. 45, 1019–1024 (1993).CrossRefGoogle Scholar
  29. 29.
    J. Krause and G. D. Ruxton, Living in Groups (Oxford University Press, Oxford, 2002), pp. 6–40.Google Scholar
  30. 30.
    M. Laitinen, R. Siddall and E. T. Valtonen, “Bioelectric Monitoring of Parasite-Induced Stress in Brown Trout and Roach,” J. Fish Biol. 48, 228–241 (1996).CrossRefGoogle Scholar
  31. 31.
    W. C. Legett, “The Role of Migration in the Life History Evolution of Fish,” Contrib. Mar. Sci. 27, 277–295 (1985).Google Scholar
  32. 32.
    S. L. Lima and L. M. Dill, “Behavioral Decisions Made under the Risk of Predation: A Review and Prospectus,” Can. J. Zool. 68, 619–640 (1990).Google Scholar
  33. 33.
    A. E. Magurran, “The Inheritance and Development of Minnow Antipredator Behaviour,” Anim. Behav. 39, 834–842 (1990).CrossRefGoogle Scholar
  34. 34.
    A. E. Magurran and T. J. Pitcher, “Provenance, Shoal Size and the Sociobiology of Predator-Evasion Behaviour in Minnow Shoals,” Proc. R. Soc. London, B 229, 439–465 (1987).Google Scholar
  35. 35.
    B. P. Manteifel, Behavioural Ecology of Animals (Nauka, Moscow, 1980), p. 295 [in Russian].Google Scholar
  36. 36.
    B. P. Manteifel, I. I. Girsa, T. S. Leshcheva, and D. S. Pavlov, “The Influence of Changing Illumination on the Formation and Decomposition of Fish Shoals,” in Feeding of Piscivorous Fish and their Relationships with their Prey, Ed. by B.P. Manteifel (Nauka, Moscow, 1965), pp. 35–38.Google Scholar
  37. 37.
    A. Mathis and R. J. F. Smith, “Chemical Alarm Signals Increase the Survival Time of Fathead Minnows (Pimephales promelas) during Encounters with Northern Pike (Esox lucius),” Behav. Ecol. 4, 260–265 (1993).CrossRefGoogle Scholar
  38. 38.
    V. N. Mikheev, Habitat Heterogeneity and Trophic Relations among Fish (Nauka, Moscow, 2006) [in Russian].Google Scholar
  39. 39.
    V. N. Mikheev, N. B. Metcalfe, F. A. Huntingford, and J. E. Thorpe, “Size-Related Differences in Behaviour and Spatial Distribution of Juvenile Atlantic Salmon in a Novel Environment,” J. Fish Biol. 45, 379–386 (1994).CrossRefGoogle Scholar
  40. 40.
    V. N. Mikheev, J. Wanzenbock, and A. F. Pasternak, “Effects of Predator-Induced Visual and Olfactory Cues on 0+ Perch (Perca fluviatilis L.) Foraging Behaviour,” Ecol. Freshwater Fish 15, 111–117 (2006).CrossRefGoogle Scholar
  41. 41.
    M. Milinski, “Risk of Predation of Parasitized Sticklebacks (Gasterosteus aculeatus L.) under Competition for Food,” Behaviour 93, 203–216 (1985).Google Scholar
  42. 42.
    M. Milinski, “Predation Risk and Feeding Behaviour,” in Behaviour of Teleost Fishes, 2nd ed., Ed. by T.J. Pitcher (Chapman and Hall, London, 1993), pp. 285–305.Google Scholar
  43. 43.
    J. Moore, Parasites and the Behavior of Animals (Oxford University Press, Oxford, 2002).Google Scholar
  44. 44.
    K. E. Murphy and T. J. Pitcher, “Predator Attack Motivation Influences the Inspection Behaviour of European Minnows,” J. Fish Biol. 50, 407–417 (1997).CrossRefGoogle Scholar
  45. 45.
    C. Navarro, F. de Lope, A. Marzal, and A. P. Moller, “Predation Risk, Host Immune Response, and Parasitism,” Behav. Ecol. 15, 629–635 (2004).CrossRefGoogle Scholar
  46. 46.
    R. M. Ness and S. A. Foster, “Parasite-Associated Phenotype Modifications in Threespined Sticklebacks,” Oikos 85, 127–134 (1999).Google Scholar
  47. 47.
    G. V. Nikolsky, Ecology of Fishes, 3rd ed. (Vysshaya Shkola, Moscow, 1974).Google Scholar
  48. 48.
    A. F. Pasternak and S. B. Schnack-Schiel, “Feeding Patterns of Dominant Antarctic Copepods: An Interplay of Diapause, Selectivity, and Availability of Food,” Hydrobiologia 453/454, 25–36 (2001).CrossRefGoogle Scholar
  49. 49.
    T. J. Pitcher and J. K. Parrish, “Functions of Shoaling Behaviour in Fishes,” in Behavior of Teleost Fishes, 2nd ed., Ed by T.J. Pitcher (Chapman & Hall, London, 1993), pp. 363–439.Google Scholar
  50. 50.
    R. Poulin, “Age-Dependent Effects of Parasites on Anti-Predator Responses in Two New Zealand Freshwater Fish,” Oecologia 96, 431–438 (1993).CrossRefGoogle Scholar
  51. 51.
    R. Poulin and G. J. Fitzgerald, “Risk of Parasitism and Microhabitat Selection in Juvenile Sticklebacks,” Can. J. Zool. 67, 14–18 (1989a).Google Scholar
  52. 52.
    R. Poulin and G. J. Fitzgerald, “Shoaling as an Anti-Ectoparasite Mechanism in Juvenile Sticklebacks,” Behav. Ecol. Sociobiol. 24, 251–255 (1989b).CrossRefGoogle Scholar
  53. 53.
    R. Poulin, D. J. Marcogliese, and J. D. McLaughlin, “Skin-Penetrating Parasites and the Release of Alarm Substances in Juvenile Rainbow Trout,” J. Fish Biol. 55, 47–53 (1999).CrossRefGoogle Scholar
  54. 54.
    D. V. Radakov, Fish Schooling as an Ecological Phenomenon (Nauka, Moscow, 1972) [in Russian].Google Scholar
  55. 55.
    A. Sih, “Predators and Prey Lifestyles: An Evolutionary and Ecological Overview,” in Predation: Direct and Indirect Impacts on Aquatic Communities, Ed. by W.C. Kerfoot and A. Sih (University of New England Press, Hanover, NH, 1987), pp. 203–224.Google Scholar
  56. 56.
    A. Sih, “Prey Uncertainty and the Balancing of Antipredator and Feeding Needs,” Am. Nat. 139, 1052–1069 (1992).CrossRefGoogle Scholar
  57. 57.
    A. Sih, “To Hide or not to Hide? Refuge Use in a Fluctuating Environment,” Trends Ecol. Evol. 12, 375–376 (1997).CrossRefGoogle Scholar
  58. 58.
    S. J. Shettleworth, “Varieties of Learning and Memory in Animals,” J. Exp. Psychol.: Anim. Behav. Processes 19, 5–14 (1993).CrossRefGoogle Scholar
  59. 59.
    R. J. F. Smith, “Alarm Signals in Fishes,” Rev. Fish Biol. Fish. 2, 33–63 (1992).CrossRefGoogle Scholar
  60. 60.
    R. J. F. Smith, “Avoiding and Deterring Predators,” in Behavioural Ecology of Teleost Fishes, Ed. by J.-G.J. Godin (Oxford University, Oxford, 1997), pp. 63–190.Google Scholar
  61. 61.
    J. Stamps, “Motor Learning and the Value of Familiar Space,” Am. Nat. 146, 41–58 (1995).CrossRefGoogle Scholar
  62. 62.
    D. W. Stephens, “Learning and Behavioral Ecology: Incomplete Information and Environmental Predictability,” in Insect Learning: Ecological and Evolutionary Perspectives, Ed. by D.R. Papaj and A.C. Lewis (Chapman & Hall, New York, 1993), pp. 195–218.Google Scholar
  63. 63.
    M. D. Suboski, S. Bain, A. E. Carty, L. M. McQuoid, M. I. Seelen, and M. Seifert, “Alarm Reaction in Acquisition and Social Transmission of Simulated-Predator Recognition by Zebra Danio Fish (Brachydanio rerio),” J. Comp. Psychol. 104, 101–112 (1990).CrossRefGoogle Scholar
  64. 64.
    A. C. Utne-Palm, “Response of Naive Two-Spotted Gobies Gobiusculus flavescens to Visual and Chemical Stimuli of their Natural Predator, Cod Gadus morhua,” Mar. Ecol. Progr. Ser. 218, 267–274 (2001).Google Scholar
  65. 65.
    D. Wakelin, Immunology to Parasites, 2nd ed. (Cambridge University, Cambridge, 1996).Google Scholar
  66. 66.
    C. Wedekind and M. Milinski, “Do Three-Spined Sticklebacks Avoid Consuming Copepods, the First Intermediate Host of Schistocephalus solidus? — an Experimental Analysis of Behavioural Resistance,” Parasitology 112, 371–383 (1996).Google Scholar
  67. 67.
    A. J. W. Ward, D. J. Hoare, I. D. Couzin, M. Broom, and J. Krause, “The Effects of Parasitism and Body Length on Positioning within Wild Fish Shoals,” J. Anim. Ecol. 71, 10–14 (2002).CrossRefGoogle Scholar
  68. 68.
    J. Williams-Howze, “Dormancy in the Free-Living Copepod Orders Cyclopoida, Calanoida and Harpacticoida,” Oceanogr. Mar. Biol. Ann. Rev. 35, 257–321 (1997).Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2006

Authors and Affiliations

  • V. N. Mikheev
    • 1
  • A. F. Pasternak
    • 2
  1. 1.Severtsov Institute of Ecology and EvolutionRussian Academy of SciencesMoscowRussia
  2. 2.Institute of OceanologyRussian Academy of SciencesMoscowRussia

Personalised recommendations