Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae
- 770 Downloads
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.
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.
KeywordsParasitic 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.
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).
- Dawkins R (1982) The extended phenotype. Oxford University Press, OxfordGoogle Scholar
- 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
- 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
- Northcote TG (1957) Common diseases and parasites of freshwater fishes in British Columbia. Management publication no. 6 of the British Columbia game commissionGoogle Scholar
- Reebs SG (2008) How fishes try to avoid predators, www.howfishbehave.ca/pdf/How%20fish%20try%20to%20avoid%20predators.pdf
- 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
- 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
- Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn and Bacon, BostonGoogle Scholar
- Therneau T (2015) A Package for Survival Analysis in S, version 2.38, http://CRAN.R-project.org/package=survival
- 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