Behavioral Ecology and Sociobiology

, Volume 69, Issue 10, pp 1723–1730 | Cite as

Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis

  • Mikhail Gopko
  • Victor N. Mikheev
  • Jouni Taskinen
Original Article

Abstract

The manipulation of host behaviour by the not-fully-developed, immature larvae of trophically transmitted parasites is attracting growing interest. A theoretical model predicts that while facilitation of host predation risk is advantageous for fully developed parasite larvae, the immature ones should make hosts less vulnerable to the predators (predation suppression hypothesis). However, there is still little evidence of such manipulation by non-infective parasite stages. We tested whether immature trematode larvae of the eye fluke, Diplostomum pseudospathaceum, a common parasite of many freshwater fishes, enhance the anti-predatory responses of their host (Oncorhynchus mykiss). To test the predation suppression hypothesis, we experimentally infected young-of-the-year (YOY) rainbow trout and studied the influence of pre-infective metacercariae of the eye fluke on the anti-predator behaviour of the fish. Fish activity, depth preference and the ability to avoid simulated predation were evaluated in the experiments. Infected fish—harbouring a moderate number of immature metacercariae—were significantly less vulnerable to simulated predation (dip-net catch) and less active (horizontal move), but their swimming depth (vertical position) was not changed when compared with the control fish harbouring no larvae. Our findings suggest that immature larvae of D. pseudospathaceum induce changes in host behaviour that can protect them from predation, thereby supporting the predation suppression hypothesis and indicating that manipulations caused by immature parasites may play an important role in modulating predator–prey interactions.

Keywords

Diplostomum Fish behaviour Host–parasite interaction Immature parasites Parasitic manipulations Rainbow trout 

References

  1. Adamo SA (2012) The strings of the puppet master: how parasites change host behavior. In: Hughes DP, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford University Press, Oxford, UK, pp 36–53CrossRefGoogle Scholar
  2. Anderson RA, Koella JC, Hurd H (1999) The effect of Plasmodium yoelii nigeriensis infection on the feeding persistence of Anopheles stephensi Liston throughout the sporogonic cycle. Proc R Soc Lond B 266:1729–1733CrossRefGoogle Scholar
  3. Bethel WM, Holmes JC (1974) Correlation of development of altered evasive behavior in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with the infectivity to the definitive host. J Parasitol 60:272–274CrossRefPubMedGoogle Scholar
  4. Burrows MT, Gibson RN (1995) The effects of food, predation risk and endogenous rhythmicity on the behaviour of juvenile plaice, Pleuronectes platessa L. Anim Behav 50:41–52CrossRefGoogle Scholar
  5. Cator LJ, George J, Blanford S, Murdock CC, Baker TC, Read AF, Thomas MB (2013) Manipulation’ without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites. Proc R Soc Lond B 280:20130711CrossRefGoogle Scholar
  6. Cézilly F, Perrot-Minnot M-J, Rigaud T (2014) Cooperation and conflict in host manipulation: interactions among macro-parasites and micro-organisms. Front Microbiol 5:248PubMedCentralPubMedGoogle Scholar
  7. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352Google Scholar
  8. Cieri MD, Stearns DE (1999) Reduction of grazing activity of two estuarine copepods in response to the chemical presence of a visual predator. Mar Ecol Prog Ser 177:157–163CrossRefGoogle Scholar
  9. Crowden A, Broom D (1980) Effects of eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Anim Behav 28:287–294CrossRefGoogle Scholar
  10. Dawkins R (1982) The extended phenotype. Oxford University Press, OxfordGoogle Scholar
  11. 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
  12. 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
  13. Domenici P, Turesson H, Brodersen J, Bronmark C (2008) Predator-induced morphology enhances escape locomotion in crucian carp. Proc R Soc Lond B 275:195–201CrossRefGoogle Scholar
  14. Fenton A, Rands SA (2006) The impact of parasite manipulation and predator foraging behavior on predator–prey communities. Ecology 87:2832–2841CrossRefPubMedGoogle Scholar
  15. Field JS, Irwin SWB (1995) Life-cycle description and comparison of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudobaeri (Razmaskin & Andrejak, 1978) from rainbow trout (Oncorhynchus mykiss Walbaum) maintained in identical hosts. Parasitol Res 81:505–517CrossRefPubMedGoogle Scholar
  16. Hafer N, Milinski M (2015) When parasites disagree: evidence for parasite-induced sabotage of host manipulation. Evolution 69:611–620PubMedCentralCrossRefPubMedGoogle Scholar
  17. 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
  18. 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
  19. 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
  20. Koella JC, Rieu L, Paul REL (2002) Stage-specific manipulation of a mosquito’s host-seeking behavior by the malaria parasite Plasmodium gallinaceum. Behav Ecol 13:816–820CrossRefGoogle Scholar
  21. Lafferty KD (1999) The evolution of trophic transmission. Parasitol Today 15:111–115CrossRefPubMedGoogle Scholar
  22. Lafferty KD (2008) Ecosystem consequences of fish parasites. J Fish Biol 73:2083–2093CrossRefGoogle Scholar
  23. Lafferty KD, Kuris MA (2012) Ecological consequences of manipulative parasites. In: Hughes DP, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford University Press, Oxford, pp 158–168CrossRefGoogle Scholar
  24. Lafferty KD, Morris AK (1996) Altered behaviour of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390–1397CrossRefGoogle Scholar
  25. Lawrence BJ, Smith RJF (1989) Behavioural response of solitary fathead minnows, Pimephales promelas, to alarm substance. J Chem Ecol 15:209–219CrossRefPubMedGoogle Scholar
  26. Lefévre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24:41–48CrossRefPubMedGoogle Scholar
  27. Lehtiniemi M (2005) Swim or hide: predator cues cause species specific reactions in young fish larvae. J Fish Biol 66:1285–1299CrossRefGoogle Scholar
  28. Levri EP, Lively CM (1996) The effect of size, reproductive condition, and parasitism on foraging behaviour in a freshwater snail, Potamopyrgus antipodarum. Anim Behav 51:891–901CrossRefGoogle Scholar
  29. 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
  30. Matthews KR, Berg NH (1997) Rainbow trout responses to water temperature and dissolved oxygen stress in two southern California stream pools. J Fish Biol 50:50–67CrossRefGoogle Scholar
  31. 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
  32. Mikheev VN, Pasternak AF, Valtonen ET (2014) Increased ventilation by fish leads to a higher risk of parasitism. Parasite Vector 7:281CrossRefGoogle Scholar
  33. 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
  34. Pettersson LB, Brönmark C (1999) Energetic consequences of an inducible morphological defence in crucian carp. Oecologia 121:12–18CrossRefGoogle Scholar
  35. Poulin R (1994) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109:S109–S118CrossRefPubMedGoogle Scholar
  36. Poulin R (1995) “Adaptive” change in the behaviour of parasitized animals: a critical review. Int J Parasitol 25:1371–1383CrossRefPubMedGoogle Scholar
  37. Poulin R (2010) Parasite manipulation of host behaviour: an update and frequently asked questions. HJ Brockmann (ed) Adv Stud Behav 41:151–186CrossRefGoogle Scholar
  38. Sato T, Watanabe K, Kanaiwa M, Niizuma Y, Harada Y, Lafferty KD (2011) Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92:201–207CrossRefPubMedGoogle Scholar
  39. Seppälä O, Jokela J (2008) Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biol Lett 4:663–666PubMedCentralCrossRefPubMedGoogle Scholar
  40. 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
  41. Seppälä O, Karvonen A, Valtonen ET (2005a) Impaired crypsis of fish infected with a trophically transmitted parasite. Anim Behav 70:895–900CrossRefGoogle Scholar
  42. 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
  43. Seppälä O, Karvonen A, Valtonen ET (2008) Shoaling behavior of fish under parasitism and predation risk. Anim Behav 75:145–150CrossRefGoogle Scholar
  44. Seppälä O, Karvonen A, Valtonen ET (2012) Behavioural mechanisms underlying ‘specific’ host manipulation by a trophically transmitted parasite. Evol Ecol Res 14:73–81Google Scholar
  45. Shirakashi S, Goater CP (2005) Chronology of parasite-induced alteration of fish behaviour: effects of parasite maturation and host experience. Parasitology 130:177–183CrossRefPubMedGoogle Scholar
  46. 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
  47. 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
  48. Sweeting R (1974) Investigations into natural and experimental infections of freshwater fish by the common eye-fluke Diplostomum spathaceum Rud. Parasitology 69:291–300CrossRefPubMedGoogle Scholar
  49. Thomas F, Schmidt-Rhaesa A, Martin G, Manu C, Durand P, Renaud F (2002) Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? J Evol Biol 153:356–361CrossRefGoogle Scholar
  50. Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199CrossRefGoogle Scholar
  51. Tierney JF, Huntingford FA, Crompton DWT (1993) The relationship between infectivity of Schistocephalus solidus (Cestoda) and anti-predator behaviour of its host, the three-spined stickleback, Gasterosteus aculeatus. Anim Behav 46:603–605CrossRefGoogle Scholar
  52. 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
  53. Voutilainen A, Taskinen J, Huuskonen H (2010) Temperature-dependent effect of the trematode eye flukes Diplostomum spp. on the growth of Arctic charr Salvelinus alpinus (L.). B Eur Assoc Fish Pat 30:106–113Google Scholar
  54. 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

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Mikhail Gopko
    • 1
  • Victor N. Mikheev
    • 1
  • Jouni Taskinen
    • 2
  1. 1.A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Laboratory for Behaviour of Lower VertebratesMoscowRussia
  2. 2.Department of Biological and Environmental SciencesUniversity of JyväskyläJyväskyläFinland

Personalised recommendations