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Altered neuronal activity in the visual processing region of eye-fluke-infected fish

Published online by Cambridge University Press:  16 October 2020

Anthony Stumbo
Affiliation:
Otago Museum, 419 Great King St., Dunedin9016, New Zealand Department of Zoology, University of Otago, 340 Great King St., Dunedin9016, New Zealand
Robert Poulin
Affiliation:
Department of Zoology, University of Otago, 340 Great King St., Dunedin9016, New Zealand
Brandon Ruehle*
Affiliation:
Department of Zoology, University of Otago, 340 Great King St., Dunedin9016, New Zealand
*
Author for correspondence: Brandon Ruehle, E-mail: brandon.ruehle90@gmail.com

Abstract

Fish, like most vertebrates, are dependent on vision to varying degrees for a variety of behaviours such as predator avoidance and foraging. Disruption of this key sensory system therefore should have some impact on the ability of fish to execute these tasks. Eye-flukes, such as Tylodelphys darbyi, often infect fish where they are known to inflict varying degrees of visual impairment. In New Zealand, T. darbyi infects the eyes of Gobiomorphus cotidianus, a freshwater fish, where it resides in the vitreous chamber between the lens and retina. Here, we investigate whether the presence of the parasite in the eye has an impact on neuronal information transfer using the c-Fos gene as a proxy for neuron activation. We hypothesized that the parasite would reduce visual information entering the eye and therefore result in lower c-Fos expression. Interestingly, however, c-Fos expression increased with T. darbyi intensity when fish were exposed to flashes of light. Our results suggest a mechanism for parasite-induced visual disruption when no obvious pathology is caused by infection. The more T. darbyi present the more visual stimuli the fish is presented with, and as such may experience difficulties in distinguishing various features of its external environment.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Almeida, O, Felix, AS, Oliveira, GA, Lopes, JS and Oliveira, RF (2019) Fighting assessment triggers rapid changes in activity of the brain social decision-making network of cichlid fish. Frontiers in Behavioral Neuroscience 13, 229.CrossRefGoogle ScholarPubMed
Baraban, SC, Taylor, MR, Castro, PA and Baier, H (2005) Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 131, 759768.CrossRefGoogle ScholarPubMed
Ben-Simon, A, Ben-Shahar, O, Vasserman, G, Ben-Tov, M and Segev, R (2012) Visual acuity in the archerfish: behavior, anatomy, and neurophysiology. Journal of Vision 12, 1818.CrossRefGoogle ScholarPubMed
Berdoy, M, Webster, JP and Macdonald, DW (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proceedings of the Royal Society B: Biological Sciences 267, 15911594.CrossRefGoogle ScholarPubMed
Blasco-Costa, I and Locke, SA (2017) Life history, systematics, and evolution of the Diplostomoidea Poirier, 1886: progress, promises and challenges emerging from molecular studies. Advances in Parasitology 98, 167225.CrossRefGoogle ScholarPubMed
Blasco-Costa, I, Poulin, R and Presswell, B (2017) Morphological description and molecular analyses of Tylodelphys sp. (Trematoda: Diplostomidae) newly recorded from the freshwater fish Gobiomorphus cotidianus (common bully) in New Zealand. Journal of Helminthology 91, 332345.CrossRefGoogle Scholar
Bosch, TJ, Maslam, S and Roberts, BL (2001) Fos-like immunohistochemical identification of neurons active during the startle response of the rainbow trout. The Journal of Comparative Neurology 439, 306314.CrossRefGoogle ScholarPubMed
Carandini, M (2000) Visual cortex: fatigue and adaptation. Current Biology 10, R605R607.CrossRefGoogle ScholarPubMed
Chappell, L (1995) The biology of diplostomatid eyeflukes of fishes. Journal of Helminthology 69, 97.CrossRefGoogle ScholarPubMed
Dragunow, M and Faull, R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. Journal of Neuroscience Methods 29, 261265.CrossRefGoogle ScholarPubMed
Grobbelaar, A, van As, LL, van As, JG and Butler, HJB (2015) Pathology of eyes and brain of fish infected with diplostomids, Southern Africa. African Zoology 50, 181186.CrossRefGoogle Scholar
Guthrie, DM (1986) Role of vision in fish behaviour. In Pitcher, TJ (ed.), The Behaviour of Teleost Fishes. Boston, MA: Springer US, pp. 75113.CrossRefGoogle Scholar
Hirsch, J and Curcio, CA (1989) The spatial resolution capacity of human foveal retina. Vision Research 29, 10951101.CrossRefGoogle ScholarPubMed
House, PK, Vyas, A and Sapolsky, R (2011) Predator cat odors activate sexual arousal pathways in brains of Toxoplasma gondii infected rats. PLoS ONE 6, e23277.CrossRefGoogle ScholarPubMed
Karvonen, A, Seppälä, O and Valtonen, ET (2004) Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129, 473478.CrossRefGoogle ScholarPubMed
Knudsen, R, Klemetsen, A, Amundsen, P-A and Hermansen, B (2006) Incipient speciation through niche expansion: an example from the Arctic charr in a subarctic lake. Proceedings of The Royal Society: Biological sciences 273, 22912298.Google Scholar
Kohler, K, Zrenner, E and Weiler, R (1995) Ethambutol alters spinuletype synaptic connections and induces morphologic alterations in the cone pedicles of the fish retina. Investigative Ophthalmology & Visual Science 36, 10461055.Google ScholarPubMed
Levine, MW (2011) Vision inner retina and ganglion cells. In Encyclopedia of Fish Physiology: From Genome to Environment. Chicago, IL: Academic Press, pp. 123130. doi: 10.1016/B978-0-12-374553-8.00092-7.CrossRefGoogle Scholar
Locke, SA, Van Dam, A, Caffara, M, Pinto, HA, Lopez-Hernandez, D and Blanar, CA (2018) Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. International Journal for Parasitology 48, 10431059.CrossRefGoogle ScholarPubMed
Maffei, L, Fiorentini, A and Bisti, S (1973) Neural correlate of perceptual adaptation to gratings. Science 182, 10361038.CrossRefGoogle ScholarPubMed
McDowall, RM (1990) New Zealand Freshwater Fishes: A Natural History and Guide. Auckland: Heinemann Reed MAF Publishing Group.Google Scholar
Morales-Montor, J, Arrieta, I, Del Castillo, LI, Rodríguez-Dorantes, M, Cerbón, MA and Larralde, C (2004) Remote sensing of intraperitoneal parasitism by the hosts brain: regional changes of c-Fos gene expression in the brain of feminized cysticercotic male mice. Parasitology 128, 343351.CrossRefGoogle ScholarPubMed
Muñoz, JCV, Staaks, G and Knopf, K (2017) The eye fluke Tylodelphys clavata affects prey detection and intraspecific competition of European perch (Perca fluviatilis). Parasitology Research 116, 25612567.CrossRefGoogle Scholar
Muñoz, JCV, Bierbach, D and Knopf, K (2019) Eye fluke (Tylodelphys clavata) infection impairs visual ability and hampers foraging success in European perch. Parasitology Research 118, 25312541.CrossRefGoogle Scholar
Northmore, D (2011) Vision optic tectum. In Encyclopedia of Fish Physiology: From Genome to Environment. Chicago, IL: Academic Press, pp. 131142. doi: 10.1016/B978-0-12-374553-8.00093-9.CrossRefGoogle Scholar
Northmore, DPM, Williams, B and Vanegas, H (1983) The teleostean torus longitudinalis: responses related to eye movements, visuotopic mapping, and functional relations with the optic tectum. Journal of Comparative Physiology 150, 3950.CrossRefGoogle Scholar
Owen, SF, Barber, I and Hart, PJB (1993) Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. Journal of Fish Biology 42, 803806.CrossRefGoogle Scholar
Pacheco, AT, Tilden, EI, Grutzner, SM, Lane, BJ, Wu, Y, Hengen, KB, Gjorgjieva, J and Turrigiano, GG (2019) Rapid and active stabilization of visual firing rates across light-dark transitions. Proceedings of the National Academy of Sciences 116, 1806818077.CrossRefGoogle Scholar
Paperna, I (1991) Diseases caused by parasites in the aquaculture of warm water fish. Annual Review of Fish Diseases 1, 155194.CrossRefGoogle Scholar
Presswell, B and Blasco-Costa, I (2020) Description of Tylodelphys darbyi n. sp. (Trematoda: Diplostomidae) from the threatened Australasian crested grebe (Podiceps cristatus australis, Gould 1844) and linking of its life-cycle stages. Journal of Helminthology 94, 18.CrossRefGoogle Scholar
R Core Team (2016) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.Rproject.org/.Google Scholar
Reid, SM, Fox, MG and Whillans, TH (1999) Influence of turbidity on piscivory in largemouth bass (Micropterus salmoides). Canadian Journal of Fisheries and Aquatic Sciences 56, 13621369.CrossRefGoogle Scholar
Rowe, DK, Dean, TL, Williams, E and Smith, JP (2003) Effects of turbidity on the ability of juvenile rainbow trout, Oncorhynchus mykiss, to feed on limnetic and benthic prey in laboratory tanks. New Zealand Journal of Marine and Freshwater Research 37, 4552.CrossRefGoogle Scholar
Ruehle, B and Poulin, R (2019) No impact of a presumed manipulative parasite on the responses and susceptibility of fish to simulated predation. Ethology 125, 745754.CrossRefGoogle Scholar
Ruehle, B and Poulin, R (2020) Risky business: influence of the eye flukes on use of risky microhabitats and conspicuousness of a fish host. Parasitology Research 119, 423430.CrossRefGoogle ScholarPubMed
Salierno, JD, Snyder, NS, Murphy, AZ, Poli, M, Hall, S, Baden, D and Kane, AS (2006) Harmful algal bloom toxins alter c-Fos protein expression in the brain of killifish, Fundulus heteroclitus. Aquatic Toxicology 78, 350357.CrossRefGoogle ScholarPubMed
Seppälä, O, Karvonen, A and Valtonen, T (2004) Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke-fish interaction. Animal Behaviour 68, 257263.CrossRefGoogle Scholar
Seppälä, O, Karvonen, A and Valtonen, T (2005) Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behaviour 70, 889894.CrossRefGoogle Scholar
Seppälä, O, Karvonen, A and Valtonen, T (2008) Shoaling behaviour of fish under parasitism and predation risk. Animal Behaviour 75, 145150.CrossRefGoogle Scholar
Stumbo, AD and Poulin, R (2016) Possible mechanism of host manipulation resulting from a diel behaviour pattern of eye-dwelling parasites? Parasitology 143, 12611267.CrossRefGoogle ScholarPubMed
Topal, A, Atamanalp, M, Oruç, E, Halıcı, MB, Şişecioğlu, M, Erol, HS, Gergit, A and Yılmaz, B (2015) Neurotoxic effects of nickel chloride in the rainbow trout brain: assessment of c-Fos activity, antioxidant responses, acetylcholinesterase activity, and histopathological changes. Fish Physiology and Biochemistry 41, 625634.CrossRefGoogle ScholarPubMed
Ubels, JL, DeLong, RJ, Hoolsema, B, Wurzberger, A, Nguyen, TT, Blankespoor, HD and Blankespoor, CL (2018) Impairment of retinal function in yellow perch (Perca flavescens) by Diplostomum baeri metacercariae. International Journal of Parasitology: Parasites and Wildlife 7, 171179.Google ScholarPubMed
VanElzakker, M, Fevurly, RD, Breindel, T and Spencer, RL (2008) Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex. Learning & Memory 15, 899908.CrossRefGoogle ScholarPubMed
Voutilainen, A, Figueiredo, K and Huuskonen, H (2008) Effects of the eye fluke Diplostomum spathaceum on the energetics and feeding of Arctic charr Salvelinus alpinus. Journal of Fish Biology 73, 22282237.CrossRefGoogle Scholar
Wagner, HJ (2011) Vision | vision in fishes: An introduction. In Encyclopedia of Fish Physiology: From Genome to Environment. Chicago, IL: Academic Press, pp. 98101. doi: 10.1016/B978-0-12-374553-8.00284-7.CrossRefGoogle Scholar
Wai, MSM, Lorke, DE, Webb, SE and Yew, DT (2006) The pattern of c-fos activation in the CNS is related to behavior in the mudskipper, Periophthalmus cantonensis. Behavioural Brain Research 167, 318327.CrossRefGoogle ScholarPubMed
Wall, AE (1998) Cataracts in farmed Atlantic salmon (Salmo salar) in Ireland, Norway and Scotland from 1995 to 1997. Veterinary Record 142, 626631.CrossRefGoogle ScholarPubMed
Wiedmann, R, Rosahl, SK, Brinker, T, Samii, M and Nakamura, M (2013) Effect of acute and chronic bilateral visual deafferentation on c-Fos immunoreactivity in the visual system of adult rats. Experimental Brain Research 229, 595607.CrossRefGoogle ScholarPubMed
Williams, C ‘Sea’ R and Whitaker, BR (1997) The evaluation and treatment of common ocular disorders in teleosts. Seminars in Avian and Exotic Pet Medicine 6, 160169.CrossRefGoogle Scholar
Wullimann, MF (1994) The teleostean torus longitudinalis: a short review on its structure, histochemistry, connectivity, possible function and phylogeny. European Journal of Morphology 32, 235242.Google Scholar