Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae

  • Mikhail GopkoEmail author
  • Victor N. Mikheev
  • Jouni Taskinen
Original Article


Parasites can manipulate their host’s behavior in order to increase their own fitness. When a parasite is trophically transmitted, it can alter the host’s anti-predatory behavior to make it more susceptible to the next host in the lifecycle. We experimentally infected young-of-the-year rainbow trout, Oncorhynchus mykiss, with realistic, naturally occurring numbers of the common eye fluke, Diplostomum pseudospathaceum, to investigate whether these parasites alter fish activity, depth preference, and activity resumption latency following a simulated avian predation attack. Behavioral tests for the first two common anti-predatory behavioral traits, which are closely related to the host’s conspicuousness to the fish-eating bird (the final host of the parasite), were performed after the parasites had attained maturity (>4 weeks post-infection). In activity latency, we also studied potential conflict between mature and immature parasites. The fish harboring mature metacercariae increased their activity, preferred to stay closer to the water surface, and spent less time immobile after the simulated avian predator attack compared to the control fish. We did not find evidence of intraspecific conflict between mature and immature eye fluke metacercariae. Interestingly, these behavioral changes did not correlate with infection intensity. Our results suggest that the D. pseudospathaceum metacercariae can change rainbow trout’s behavior predisposing them to avian predation. Since eye flukes are common freshwater fish parasites, the resulting behavioral changes caused by these parasites likely play an important role in freshwater food webs.

Significance statement

By sabotaging the intermediate host’s anti-predatory behavioral traits, a parasite can predispose the host to predation by the final host. We experimentally studied whether the parasitic eye fluke, Diplostomum pseudospathaceum, alters rainbow trout’s anti-predatory behavior. Infected fish were more active, preferred upper water layers, and recovered quickly from the simulated avian predator attack compared to control fish. Our results suggest that the eye fluke changes its host’s behavior in order to make it more vulnerable to the final host. Most importantly, the observed behavioral changes arose, when the infection intensity was similar to rates found in natural conditions. This implies that, in natural conditions, eye flukes can substantially alter host anti-predatory defenses and affect predator–prey interactions.


Parasitic manipulations Anti-predatory behavior Experimental infections Diplostomum pseudospathaceum Host–parasite interaction 



We cordially thank two anonymous referees for their constructive comments and suggestions. We are also very grateful to Prof. Roger Jones and Punidan Jeyasingh for reading and editing a draft of this manuscript.

This work was supported by the Academy of Finland mobility grant 279220/2014 to JT, the CIMO Fellowship grant TM-14-9506 to JT, and the RFBR grant 14-04-00090a to VM.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

The experiments were conducted with the permission of the Centre for Economic Development, Transport, and Environment of South Finland (license number ESAVI/6759/04.10.03/2011).

Supplementary material

265_2017_2300_MOESM1_ESM.doc (34 kb)
ESM 1 (DOC 34 kb)
265_2017_2300_MOESM2_ESM.xlsx (18 kb)
ESM 2 (XLSX 18 kb)


  1. Bethel WM, Holmes JC (1973) Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths. J Parasitol 59:945–956CrossRefGoogle Scholar
  2. Brown GE, Dreier VM (2002) Predator inspections behavior and attack cone avoidance in a characin fish: the effects of predator diet and prey experience. Anim Behav 63:1175–1181CrossRefGoogle Scholar
  3. Cézilly F, Favrat A, Perrot-Minnot M-J (2013) Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects. J Exp Biol 216:27–35CrossRefPubMedGoogle Scholar
  4. Cézilly F, Perrot-Minnot M-J, Rigaud T (2014) Cooperation and conflict in host manipulation: interactions among macro-parasites and micro-organisms. Front Microbiol 5:248PubMedPubMedCentralGoogle Scholar
  5. Coats J, Poulin R, Nakagawa S (2010) The consequences of parasitic infections for host behavioural correlations and repeatability. Behaviour 147:367–382CrossRefGoogle Scholar
  6. Crowden A, Broom D (1980) Effects of eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Anim Behav 28:287–294CrossRefGoogle Scholar
  7. Curtis LA (1987) Vertical distribution of an estuarine snail altered by a parasite. Science 235:1509–1511CrossRefPubMedGoogle Scholar
  8. Dawkins R (1982) The extended phenotype. Oxford University Press, OxfordGoogle Scholar
  9. Désilets HD, Locke SA, McLaughlin JD, Marcogliese DJ (2013) Community structure of Diplostomum spp. (Digenea: Diplostomidae) in eyes of fish: main determinants and potential interspecific interactions. Int J Parasitol 43:929–939CrossRefPubMedGoogle Scholar
  10. Dianne L, Perrot-Minnot M-J, Bauer A, Gaillard M, Léger E, Rigaud T (2011) Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65:2692–2698CrossRefPubMedGoogle Scholar
  11. Engström-Öst J, Lehtiniemi M (2004) Threat-sensitive predator avoidance by pike larvae. J Fish Biol 65:251–261CrossRefGoogle Scholar
  12. Evans AF, Hostetter NJ, Roby DD, Collis K, Lyons DE, Sandford BP, Ledgerwood RD, Sebring S (2012) Systemwide evaluation of avian predation on juvenile salmonids from the Columbia River based on recoveries of passive integrated transponder tags. T Am Fish Soc 141:975–989CrossRefGoogle Scholar
  13. Franceschi N, Cornet S, Bollache L, Dechaume-Moncharmont FX, Bauer A, Motreuil S, Rigaud T (2010) Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation. Evolution 64:2417–2430PubMedGoogle Scholar
  14. Fredensborg BL, Longoria AN (2012) Increased surfacing behavior in longnose killifish infected by brain-encysting trematode. J Parasitol 98:899–903CrossRefPubMedGoogle Scholar
  15. Goel MK, Khanna P, Kishore J (2010) Understanding survival analysis: Kaplan-Meier estimate. Int J Ayurveda Res 1:274CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gopko MV, Mikheev VN, Taskinen J (2015) Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis. Behavioral Ecol Sociobiol 69:1723–1730CrossRefGoogle Scholar
  17. Hafer N, Milinski M (2015) When parasites disagree: evidence for parasite-induced sabotage of host manipulation. Evolution 69:611–620CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hafer N, Milinski M (2016) Inter- and intraspecific conflicts between parasites over host manipulation. Proc R Soc B 283:20152870CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hammerschmidt K, Koch K, Milinski M, Chubb JC, Parker GA (2009) When to go: optimization of host switching in parasites with complex life cycles. Evolution 63:1976–1986CrossRefPubMedGoogle Scholar
  20. Hemmi JM, Pfeil A (2010) A multi-stage anti-predator response increases information on predation risk. J Exp Biol 213:1484–1489CrossRefPubMedGoogle Scholar
  21. Höglund J, Thuvander A (1990) Indications of nonspecific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis. Dis Aquat Org 8:91–97CrossRefGoogle Scholar
  22. James CT, Noyes KJ, Stumbo AD, Wisenden BD, Goater CP (2008) Cost of exposure to trematode cercariae and learned recognition and avoidance of parasitism risk by fathead minnows. J Fish Biol 73:2238–2248CrossRefGoogle Scholar
  23. Karvonen A, Seppälä O, Valtonen ET (2004) Eye fluke induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129:473–478CrossRefPubMedGoogle Scholar
  24. Karvonen A, Paukku S, Seppälä O, Valtonen ET (2005) Resistance against eye flukes: naïve versus previously infected fish. Parasitol Res 95:55–59CrossRefPubMedGoogle Scholar
  25. Kekäläinen J, Lai Y-T, Vainikka A, Sirkka I, Kortet R (2014) Do brain parasites alter host personality?—experimental study in minnows. Behav Ecol Sociobiol 68:197–204CrossRefGoogle Scholar
  26. Kortet R, Rantala MJ, Hedrick A (2007) Boldness in anti-predator behavior and immune defence in field crickets. Evol Ecol Res 9:185–197Google Scholar
  27. Krause J, Godin J-GJ (1995) Predator preferences for attacking particular prey group sizes: consequences for predator hunting success and prey predation risk. Anim Behav 50:465–473CrossRefGoogle Scholar
  28. Krause J, Godin J-GJ, Rubenstein DI (1998) Group choice as a function of group size difference and assessment time in fish: the influence of species vulnerability to predation. Ethology 104:68–74CrossRefGoogle Scholar
  29. Lafferty KD, Morris AK (1996) Altered behaviour of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390–1397CrossRefGoogle Scholar
  30. Lafferty KD, Shaw JC (2013) Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 216:56–66CrossRefPubMedGoogle Scholar
  31. Langerhans RB (2006) Evolutionary consequences of predation: avoidance, escape, reproduction, and diversification. In: Elewa AMT (ed) Predation in organisms: a distinct phenomenon. Springer-Verlag, Heidelberg, pp 177–220Google Scholar
  32. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  33. Louhi KR, Karvonen A, Rellstab C, Jokela J (2010) Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Infect Genet Evol 10:1271–1277CrossRefPubMedGoogle Scholar
  34. Marcogliese DJ, Dumont P, Gendron AD, Mailhot Y, Bergeron E, McLaughlin JD (2001) Spatial and temporal variation in abundance of Diplostomum spp. in walleye (Stizostedion vitreum) and white suckers (Catostomus commersoni) from the St. Lawrence River. Can J Zool 79:355–369CrossRefGoogle Scholar
  35. Mikheev V, Pasternak A, Taskinen J, Valtonen ET (2010) Parasite-induced aggression and impaired contest ability in a fish host. Parasite Vector 3:17CrossRefGoogle Scholar
  36. Miura O, Chiba S (2007) Effects of trematode double infection on the shell size and distribution of snail hosts. Parasitol Int 56:19–22CrossRefPubMedGoogle Scholar
  37. Miura O, Kuris AM, Torchin ME, Hechinger RF, Chiba S (2006) Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proc R Soc Lond B 273:1323–1328CrossRefGoogle Scholar
  38. Moore J (2013) An overview of parasite-induced behavioral alterations—and some lessons from bats. J Exp Biol 216:11–17CrossRefPubMedGoogle Scholar
  39. Northcote TG (1957) Common diseases and parasites of freshwater fishes in British Columbia. Management publication no. 6 of the British Columbia game commissionGoogle Scholar
  40. Owen SF, Barber I, Hart PJB (1993) Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 42:803–806CrossRefGoogle Scholar
  41. Parker GA, Ball MA, Chubb JC, Hammerschmidt K, Milinski M (2009) When should a trophically transmitted parasite manipulate its host? Evolution 63:448–458CrossRefPubMedGoogle Scholar
  42. Poulin R (1994) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109:S109–S118CrossRefPubMedGoogle Scholar
  43. Poulin R (2010) Parasite manipulation of host behaviour: an update and frequently asked questions. Adv Stud Behav 41:151–186CrossRefGoogle Scholar
  44. Poulin R (2013) Parasite manipulation of host personality and behavioural syndromes. J Exp Biol 216:18–26CrossRefPubMedGoogle Scholar
  45. Poulin R, Fredensborg BL, Hansen E, Leung TLF (2005) The true cost of host manipulation by parasites. Behav Process 68:241–244CrossRefGoogle Scholar
  46. Pulkkinen K, Pasternak AF, Hasu T, Valtonen ET (2000) Effect of Triaenophorus crassus (Cestoda) infection on behaviour and susceptibility to predation of the first intermediate host Cyclops strenuus (Copepoda). J Parasitol 86:664–670CrossRefPubMedGoogle Scholar
  47. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Google Scholar
  48. Reebs SG (2008) How fishes try to avoid predators,
  49. Rellstab C, Louhi KR, Karvonen A, Jokela J (2011) Analysis of trematode parasite communities in fish eye lenses by pyrosequencing of naturally pooled DNA. Infect Genet Evol 11:1276–1286CrossRefPubMedGoogle Scholar
  50. Rusticus S, Lovato CY (2014) Impact of sample size and variability on the power and type I error rates of equivalence test: a simulation study. PARE 11:1–10Google Scholar
  51. Schielzeth H, Nakagawa S (2013) Nested by design: model fitting and interpretation in a mixed model era. Method Ecol Evol 4:14–24CrossRefGoogle Scholar
  52. Selbach C, Soldánová M, Georgieva S, Kostadinova A, Sures B (2015) Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi’ species complex. Parasit Vectors 8:300. doi: 10.1186/s13071-015-0904-4
  53. Seppälä O, Karvonen A, Valtonen ET (2004) Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Anim Behav 68:257–263CrossRefGoogle Scholar
  54. Seppälä O, Karvonen A, Valtonen ET (2005a) Impaired crypsis of fish infected with a trophically transmitted parasite. Anim Behav 70:895–900CrossRefGoogle Scholar
  55. Seppälä O, Karvonen A, Valtonen ET (2005b) Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Anim Behav 70:889–894CrossRefGoogle Scholar
  56. Seppälä O, Karvonen A, Valtonen ET (2006) Susceptibility of eye fluke-infected fish to predation by bird hosts. Parasitology 132:575–579CrossRefPubMedGoogle Scholar
  57. Seppälä O, Karvonen A, Valtonen ET (2008) Shoaling behavior of fish under parasitism and predation risk. Anim Behav 75:145–150CrossRefGoogle Scholar
  58. Sogard SM, Olla BL (1996) Food deprivation affects vertical distribution and activity of a marine fish in a thermal gradient: potential energy-conserving mechanisms. Mar Ecol-Prog Ser 133:43–55CrossRefGoogle Scholar
  59. Sokolov SG (2010) Parasites of underyearling kamchatka mykiss Parasalmo mykiss mykiss (Osteichithyes: Salmonidae) in the Utkholok River (North-western Kamchatka). Parazitologiia 44:336–342 (in Russian)PubMedGoogle Scholar
  60. Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn and Bacon, BostonGoogle Scholar
  61. Therneau T (2015) A Package for Survival Analysis in S, version 2.38,
  62. Thomas F, Fauchier J, Laffery K (2002) Conflict of interest between a nematode and a trematode in an amphipod host: test of the ‘sabotage’ hypothesis. Behav Ecol Sociobiol 51:296–301CrossRefGoogle Scholar
  63. Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199CrossRefGoogle Scholar
  64. Urdal K, Tierney JF, Jakobsen PJ (1995) The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. J Parasitol 81:330–333CrossRefPubMedGoogle Scholar
  65. Valtonen ET, Gibson DI (1997) Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities of northern Finland. Ann Zool Fenn 34:47–59Google Scholar
  66. Voellmy IK, Purser J, Simpson SD, Radford AN (2014) Increased noise levels have different impacts on the anti-predator behaviour of two sympatric fish species. PLoS One 9:e102946CrossRefPubMedPubMedCentralGoogle Scholar
  67. Vyas A, Kim SK, Sapolsky RM (2007) The effects of Toxoplasma infection on rodent behavior are dependent on dose of the stimulus. Neuroscience 148:342–348CrossRefPubMedPubMedCentralGoogle Scholar
  68. Webster JP (1994) The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology 109:583–589CrossRefPubMedGoogle Scholar
  69. Webster JP (2007) The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophrenia Bull 33:752–756CrossRefGoogle Scholar
  70. Weinersmith KL, Warinner CB, Tan V, Harris DJ, Mora AB, Kuris AM, Lafferty KD, Hechinger RF (2014) A lack of crowding? Body size does not decrease with density for two behavior-manipulating parasites. Integr Comp Biol 54:184–192CrossRefPubMedGoogle Scholar
  71. Weinreich F, Benesh DP, Milinski M (2013) Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective. Parasitology 140:129–135CrossRefPubMedGoogle Scholar
  72. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.A.N. Severtsov Institute of Ecology and Evolution, (RAS), Laboratory for Behaviour of Lower VertebratesMoscowRussia
  2. 2.Department of Biological and Environmental SciencesUniversity of JyväskyläJyväskyläFinland

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