Abstract
Visual performance and environmental conditions can influence both behavioral patterns and predator-prey interactions of fish. Eye parasites can impair their host’s sensory performance with important consequences for the detection of prey, predators, and conspecifics. We used European perch (Perca fluviatilis) experimentally infected with the eye fluke Tylodelphys clavata and evaluated their feeding behavior and competitive ability under competition with non-infected conspecifics, in groups of four individuals, for two different prey species (Asellus aquaticus and Daphnia magna). To test whether the effect of T. clavata infection differs at different light conditions, we performed the experiments at two light intensities (600 and 6 lx). Foraging efficiency of perch was significantly affected by infection but not by light intensity. The distance at which infected fish attacked both prey species was significantly shorter in comparison to non-infected conspecifics. Additionally, infected fish more often unsuccessfully attacked A. aquaticus. Although the outcome of competition depended on prey species, there was a general tendency that non-infected fish consumed more of the available prey under both light intensities. Even though individual prey preferences for either A. aquaticus or D. magna were observed, we could not detect that infected fish change their prey preference to compensate for a reduced competitive foraging ability. As infection of T. clavata impairs foraging efficiency and competitive ability, infected fish would need to spend more time foraging to attain similar food intake as non-infected conspecifics; this presumably increases predation risk and potentially enhances transmission success to the final host.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ali MA, Ryder RA, Anctil M (1977) Photoreceptors and visual pigments as related to behavioral responses and preferred habitats of perches (Perca spp.) and pikeperches (Stizostedion spp.). J Fish Res Board Can 34:1475–1480. https://doi.org/10.1139/f77-212
Andrikovics S (1981) Further data to daily migration of the larvae of aquatic insect. Opusc Zool 17–18:49–55
Barber I (2007) Parasites, behaviour and welfare in fish. Appl Anim Behav Sci 104:251–264. https://doi.org/10.1016/j.applanim.2006.09.005
Barber I, Huntingford FA (1995) The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 132:1223–1240. https://doi.org/10.1163/156853995X00540
Barber I, Wright HA (2005) Effects of parasites on fish behaviour: interactions with host physiology. In: Katherine RWW, Sloman A, Sigal B (eds) Fish physiology. Academic Press, San Diego, pp 109–149. https://doi.org/10.1016/S1546-5098(05)24004-9
Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: an evolutionary perspective and review. Rev Fish Biol Fish 10:131–165. https://doi.org/10.1023/A:1016658224470
Barber I, Mora AB, Payne EM, Weinersmith KL, Sih A (2017) Parasitism, personality and cognition in fish. Behav Process 141:205–219. https://doi.org/10.1016/j.beproc.2016.11.012
Bergman E (1988) Foraging abilities and niche breadths of two percids, Perca fluviatilis and Gymnocephalus cernua, under different environmental conditions. J Anim Ecol 57:443–453. https://doi.org/10.2307/4916
Brännäs E, Alanärä A, Magnhagen C (2001) The social behaviour of fish. In: Keeling LJ, Gonyou HW (eds) Social behaviour in farm animals. CABI publishing, New York, pp 275–304
Buchmann K, Moller SH, Uldal A, Bresciani J (1997) Different seasonal infection dynamics of two species of eye-flukes (Diplostomum spathaceum and Tylodelphys clavata) in rainbow trout (Oncorhynchus mykiss). Bull Eur Assoc Fish Pathol 17:165–170
Craig JF (1977) Seasonal changes in the day and night activity of adult perch, Perca fluviatilis L. J Fish Biol 11:161–166. https://doi.org/10.1111/j.1095-8649.1977.tb04109.x
Craig JF (1978) A study of the food and feeding of perch, Perca fluviatilis L., inWindermere. Freshw Biol 8:59–68. https://doi.org/10.1111/j.1365-2427.1978.tb01426.x
Craig JF (2000) Percid fishes: systematics, ecology and exploitation. Blackwell Science, Oxford
Crowden AE, Broom DM (1980) Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Anim Behav 28:287–294. https://doi.org/10.1016/S0003-3472(80)80031-5
Diehl S (1988) Foraging efficiency of three freshwater fishes: effects of structural complexity and light. Oikos 53:207–214. https://doi.org/10.2307/3566064
Eiane K, Aksnes DL, Giske J (1997) The significance of optical properties in competition among visual and tactile planktivores: a theoretical study. Ecol Model 98:123–136. https://doi.org/10.1016/S0304-3800(96)01909-6
Eklöv P (1992) Group foraging versus solitary foraging efficiency in piscivorous predators: the perch, Perca fluviatilis, and pike, Esox lucius, patterns. Anim Behav 44:313–326. https://doi.org/10.1016/0003-3472(92)90037-A
Faltýnková A, Našincová V, Kablásková L (2007) Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite 14:39–51. https://doi.org/10.1051/parasite/2007141039
Flink H, Behrens JW, Svensson PA (2017) Consequences of eye fluke infection on anti-predator behaviours in invasive round gobies in Kalmar sound. Parasitol Res 116:1653–1663. https://doi.org/10.1007/s00436-017-5439-5
Frankiewicz P, Wojtal-Frankiewicz A (2012) Two different feeding tactics of young-of-the-year perch, Perca fluviatilis L., inhabiting the littoral zone of the lowland Sulejow Reservoir (Central Poland). Ecohydrol Hydrobiol 12:35–41. https://doi.org/10.2478/v10104-012-0001-7
Gopko M, Mikheev VN, Taskinen J (2017) Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae. Behav Ecol Sociobiol 71:68. https://doi.org/10.1007/s00265-017-2300-x
Guma’a SA (1978) The food and feeding habits of young perch, Perca fluviatilis, in Windermere. Freshw Biol 8:177–187. https://doi.org/10.1111/j.1365-2427.1978.tb01439.x
Huusko A, Vuorimies O, Sutela T (1996) Temperature- and light-mediated predation by perch on vendace larvae. J Fish Biol 49:441–457. https://doi.org/10.1111/j.1095-8649.1996.tb00040.x
Jakobsen PJ, Johnsen GH, Larsson P (1988) Effects of predation risk and parasitism on the feeding ecology, habitat use, and abundance of lacustrine threespine stickleback (Gasterosteus aculeatus). Can J Fish Aquat Sci 45:426–431. https://doi.org/10.1139/f88-051
Kennedy CR (2001) Interspecific interactions between larval digeneans in the eyes of perch, Perca fluviatilis. Parasitology 122:S13–S22. https://doi.org/10.1017/S0031182000016851
Khorramshahi O, Schartau JM, Kröger RHH (2008) A complex system of ligaments and a muscle keep the crystalline lens in place in the eyes of bony fishes (teleosts). Vis Res 48:1503–1508. https://doi.org/10.1016/j.visres.2008.03.017
Kozicka J, Niewiadomska K (1960) Studies on the biology and taxonomy of trematodes of the genus Tylodelphys Diesing, 1850 (Diplostomatidae). Acta Parasitol Pol 8:379–400
Lafferty KD, Kuris AM (2012) Ecological consequences of manipulative parasites. In: Hughes DP, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford university press, Oxford, pp 158–171
Metcalfe NB (1986) Intraspecific variation in competitive ability and food intake in salmonids: consequences for energy budgets and growth rates. J Fish Biol 28:525–532. https://doi.org/10.1111/j.1095-8649.1986.tb05190.x
Mikeš L (2001) Simplified determination key, Cercariae. 1st workshop on bird schistosomes and cercarial dermatitis. Dolní Vĕstonice, Czech Republic
Milinski M (1984) Parasites determine a predator’s optimal feeding strategy. Behav Ecol Sociobiol 15:35–37. https://doi.org/10.1007/BF00310212
Moore J (2002) Parasites and behaviour of animals. Oxford series in ecology and evolution. Oxford University Press, New York, p 315
Nurminen L, Pekcan-Hekim Z, Horppila J (2010) Feeding efficiency of planktivorous perch Perca fluviatilis and roach Rutilus rutilus in varying turbidity: an individual-based approach. J Fish Biol 76:1848–1855. https://doi.org/10.1111/j.1095-8649.2010.02600.x
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 42:803–806. https://doi.org/10.1111/j.1095-8649.1993.tb00387.x
Padros F, Knuden R, Blasco-Costa I (2018) Histopathological characterisation of retinal lesions associated to Diplostomum species (Platyhelminthes: Trematoda) infection in polymorphic Arctic charr Salvelinus alpinus. Int J Parasitol 7:68–74. https://doi.org/10.1016/j.ijppaw.2018.01.007
Partridge BL, Pitcher TJ (1980) The sensory basis of fish schools: relative roles of lateral line and vision. J Comp Physiol 135(4):315–325. https://doi.org/10.1007/BF00657647
Pascoe D, Mattey D (1977) Dietary Stress in Parasitized and Non-parasitized Gasterosteus aculeatus L. Z Parasitenkd 51:179–186. https://doi.org/10.1007/BF00500957
Pekcan-Hekim Z, Joensuu L, Horppila J (2013) Predation by visual planktivore perch (Perca fluviatilis) in a turbulent and turbid environment. Can J Fish Aquat Sci 70:854–859. https://doi.org/10.1139/cjfas-2012-0466
Persson L (1983) Food consumption and competition between age classes in a perch Perca fluviatilis population in a shallow eutrophic lake. Oikos 40:197–207. https://doi.org/10.2307/3544583
Persson L (1986) Effects of reduced interspecific competition on resource utilization in perch (Perca fluviatilis). Ecology 67:355–364. https://doi.org/10.2307/1938578
Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fish. Chapman & Hall, London, pp 363–439
Poulin R (1995) “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 25:1371–1383. https://doi.org/10.1016/0020-7519(95)00100-X
Poulin R (2007) Evolutionary ecology of parasites 2nd edn. Princeton University Press, Princeton
Rahn AK, Vitt S, Drolshagen L, Scharsack JP, Rick IP, Bakker TCM (2018) Parasitic infection of the eye lens affects shoaling preferences in three-spined stickleback. Biol J Linn Soc 123(2):377–387. https://doi.org/10.1093/biolinnean/blx155
Richmond HE, Hrabik TR, Mensinger AF (2004) Light intensity, prey detection and foraging mechanisms of age 0 year yellow perch. J Fish Biol 65:195–205. https://doi.org/10.1111/j.0022-1112.2004.00444.x
Sandström A (1999) Visual ecology of fish – a review with special reference to percids. Natl Bd Fish Pub Fiskeriverket Rapp 2:45–80
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 68:257–263. https://doi.org/10.1016/j.anbehav.2003.10.021
Seppälä O, Karvonen A, Valtonen ET (2005a) Impaired crypsis of fish infected with a trophically transmitted parasite. Anim Behav 70:895–900. https://doi.org/10.1016/j.anbehav.2005.01.021
Seppälä O, Karvonen A, Valtonen ET (2005b) Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Anim Behav 70:889–894. https://doi.org/10.1016/j.anbehav.2005.01.020
Seppälä O, Karvonen A, Valtonen ET (2008) Shoaling behaviour of fish under parasitism and predation risk. Anim Behav 75:145–150. https://doi.org/10.1016/j.anbehav.2007.04.022
Seppälä O, Karvonen A, Valtonen ET (2012) Behavioural mechanisms underlying ‘specific’ host manipulation by a trophically transmitted parasite. Evol Ecol Res 14:73–81
Shariff M, Richards RH, Sommerville C (1980) The histopathology of acute and chronic infections of rainbow trout Salmo gairdneri Richardson with eye flukes, Diplostomum spp. J Fish Dis 3:455–465. https://doi.org/10.1111/j.1365-2761.1980.tb00432.x
Staffan F, Magnhagen C, Alanärä A (2002) Variation in food intake within groups of juvenile perch. J Fish Biol 60:771–774. https://doi.org/10.1111/j.1095-8649.2002.tb01702.x
Strand Å, Alanärä A, Magnhagen C (2007) Effect of group size on feed intake, growth and feed efficiency of juvenile perch. J Fish Biol 71:615–619. https://doi.org/10.1111/j.1095-8649.2007.01497.x
Stumbo AD, Poulin R (2016) Possible mechanism of host manipulation resulting from a diel behaviour pattern of eye-dwelling parasites? Parasitology 143:1261–1267. https://doi.org/10.1017/S0031182016000810
Svanbäck R, Persson L (2004) Individual diet specialization, niche width and population dynamics: implications for trophic polymorphisms. J Anim Ecol 73:973–982. https://doi.org/10.1111/j.0021-8790.2004.00868.x
Ubels JL, DeJong RJ, Hoolsema B, Wurzberger A, Nguyen T, Blankespoor HD, Blankespoor CL (2018) Impairment of retinal function in yellow perch (Perca flavescens) by Diplostomum baeri metacercariae. Int J Parasitol Parasites Wildl 7:171–179. https://doi.org/10.1016/j.ijppaw.2018.05.001
Utne ACW (1997) The effect of turbidity and illumination on the reaction distance and search time of the marine planktivore Gobiusculus flavescens. J Fish Biol 50:926–938. https://doi.org/10.1111/j.1095-8649.1997.tb01619.x
Vinyard GL, O’Brien J (1976) Effects of light and turbidity on the reactive distance of bluegill (Lepomis macrochirus). J Fish Res Board Can 33(12):2845–2849. https://doi.org/10.1139/f76-342
Vivas Muñoz JC, Staaks G, Knopf K (2017) The eye fluke Tylodelphys clavata affects prey detection and intraspecific competition of European perch (Perca fluviatilis). Parasitol Res 116:2561–2567. https://doi.org/10.1007/s00436-017-5564-1
Voutilainen A, Figueiredo K, Huuskonen H (2008) Effects of the eye fluke Diplostomum spathaceum on the energetics and feeding ofArctic charr Salvelinus alpinus. J Fish Biol 73:2228–2237. https://doi.org/10.1111/j.1095-8649.2008.02050.x
Westerberg M, Staffan F, Magnhagen C (2004) Influence of predation risk on individual competitive ability and growth in Eurasian perch, Perca fluviatilis. Anim Behav 67:273–279. https://doi.org/10.1016/j.anbehav.2003.06.003
Winfield IJ (1986) The influence of simulated aquatic macrophytes on the zooplankton consumption rate of juvenile roach, Rutilus rutilus, rudd, Scardinius erythrophthalmus, and perch, Perca fluviatilis. I J Fish Biol 29:37–48. https://doi.org/10.1111/j.1095-8649.1986.tb04997.x
Acknowledgments
We are grateful to Dr. Jasminca Behrmann-Godel for her valuable advice on raising perch in the lab and Mathias Kunow for his support in collecting fertilized eggs of perch. Further, we would like to thank Janne Ros Irmler and Amrei Gründer for their support with the videos and Dr. Sabine Hilt for her valuable comments on an earlier draft of the manuscript.
Funding
This research was supported by the Graduate School IMPact-Vector funded by the Senate Competition Committee grant (SAW-2014-SGN-3) of the Leibniz-Association. Research of D.B. is currently supported by the DFG (BI 1828/2-1).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Ethical approval
Tagging of the fish, experimental infection, and behavioral experiments were performed in accordance with the German Animal Welfare Act and were approved by the Berlin State Office for Health and Social Affairs (LaGeSo, reference number G0243/16).
Additional information
Section Editor: Astrid Holzer
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vivas Muñoz, J.C., Bierbach, D. & Knopf, K. Eye fluke (Tylodelphys clavata) infection impairs visual ability and hampers foraging success in European perch. Parasitol Res 118, 2531–2541 (2019). https://doi.org/10.1007/s00436-019-06389-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06389-5