Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-27T17:51:29.507Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of Ligula intestinalis plerocercoids (Cestoda: Diphyllobothriidea) on the occurrence of eyeflukes in roach (Rutilus rutilus) from a lake in south-east England

Published online by Cambridge University Press:  31 January 2018

N.J. Morley  and
J.W. Lewis
N.J. Morley*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
J.W. Lewis
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
*
Author for correspondence: N.J. Morley, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Vertebrate hosts commonly harbour concurrent infections of different helminth species which may interact with each other in a synergistic, antagonistic or negligible manner. Direct interactions between helminths that share a common site in the host have been regularly reported, but indirect interactions between species that occur in different sites are rarely described, especially in fish hosts. Plerocercoids of Ligula intestinalis are common infections of the peritoneal (body) cavity of roach (Rutilus rutilus) in freshwater habitats. These larval cestodes can cause extensive systemic pathologies to the fish host, which in turn may alter its susceptibility as a target host for other helminth species. The present study, using an existing dataset, investigates the influence of L. intestinalis (ligulosis) on frequently occurring eyefluke infections in roach sampled from a lake in south-east England. The occurrence of two species of eyefluke (Diplostomum sp. and Tylodelphys sp.) in the roach population demonstrated no significant levels of interaction with each other. The prevalence but not mean intensity or abundance of Diplostomum sp. was significantly increased in ligulosed roach, while the incidence of Tylodelphys sp. remained unchanged. Analyses of bilateral asymmetry in the occurrence of eyeflukes in left and right eyes of infected fish demonstrate that Tylodelphys sp. shows significant asymmetry in non-ligulosed roach, which is not replicated in ligulosed individuals. In contrast, Diplostomum sp. shows no evidence of asymmetry in either ligulosed or non-ligulosed fish.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 1 , January 2019 , pp. 66 - 70
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barber, I and Scharsack, JP (2010) The three-spined stickleback–Schistocephalus solidus system: an experimental model for investigating host–parasite interactions in fish. Parasitology 137, 411–424.Google Scholar
Benesh, DP and Kalbe, M (2016) Experimental parasite community ecology: intraspecific variation in a large tapeworm affects community assembly. Journal of Animal Ecology 85, 1004–1013.Google Scholar
Blair, D (1977) A key to cercariae of British strigeoids (Digenea) for which the life-cycles are known, and notes on the characters used. Journal of Helminthology 51, 155–166.Google Scholar
Bouillon, DR and Curtis, MA (1987) Diplostomiasis (Trematoda: Strigeidae) in arctic charr (Salvelinus alpinus) from Charr lake, northern Labrador. Journal of Wildlife Diseases 23, 502–505.Google Scholar
Burrough, RJ (1978) The population biology of two species of eyefluke, Diplostomum spathaceum and Tylodelphys clavata, in roach and rudd. Journal of Fish Biology 13, 19–32.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Chandler, P (1994) Fieldwork at Dinton Pastures to the end of 1993. British Journal of Entomology and Natural History 7, 118–126.Google Scholar
Chappell, LH (1995) The biology of diplostomatid eyeflukes of fishes. Journal of Helminthology 69, 97–101.Google Scholar
Chappell, LH, Hardie, LJ and Secombes, CJ (1994) Diplostomiasis: The disease and host–parasite interactions. pp. 59–86 in Pike, AW and Lewis, JW (Eds) Parasitic diseases of fish. Tresaith, Dyfed, Samara Publishing.Google Scholar
Christensen, NØ, Nansen, P, Fagbemi, BO and Monrad, J (1987) Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387–410.Google Scholar
Chubb, JC (1979) Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17, 142–314.Google Scholar
Combes, C, Fournier, A, Moné, H and Theron, A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3–S13.Google Scholar
Corrêa-Oliveira, R, Golgher, DB, Guilherme, CO, Carvalho, OS, Massara, CL, Caldas, IR, Colley, DG and Gazzinelli, G (2002) Infection with Schistosoma mansoni correlates with altered immune responses to Ascaris lumbricoides and hookworm. Acta Tropica 83, 123–132.Google Scholar
Cox, FEG (2001) Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38.Google Scholar
Curry, AJ, Else, KJ, Jones, F, Bancroft, A, Grencis, RK and Dunne, DW (1995) Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. Journal of Experimental Medicine 181, 769–774.Google Scholar
Dubinina, MN (1980) Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. New Delhi, Amerind.Google Scholar
Giles, N (1987) Predation risk and reduced foraging activity in fish – experiments with parasitized and non-parasitized 3-spined sticklebacks, Gasterosteus aculeatus L. Journal of Fish Biology 31, 37–44.Google Scholar
Graczyk, T (1991) Cases of bilateral asymmetry of Diplostomum pseudosapthaceum Niewiadomska, 1984 metacercariae infections (Trematoda: Diplostomatidae) in the eye lens of fish. Acta Parasitologica Polonica 36, 131–134.Google Scholar
Haas, W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349–364.Google Scholar
Haas, W, Wulff, C, Grabe, K, Meyer, V and Haeberlein, S (2007) Navigation within host tissues: cues for orientation of Diplostomum spathaceum (Trematoda) in fish towards vein, head and eye. Parasitology 134, 1013–1023.Google Scholar
Hoole, D (1994) Tapeworm infections in fish: past and present problems. pp. 119–140 in Pike, AW and Lewis, JW (Eds) Parasitic diseases of fish. Tresaith, Dyfed, Samara Publishing.Google Scholar
Hoole, D, Carter, V and Dufour, S (2010) Ligula intestinalis (Cestoda: Pseudophyllidae): an ideal fish–metazoan parasite model? Parasitology 137, 425–438.Google Scholar
Izvekova, GI and Tyutin, AV (2014) Activity of digestive enzymes and distribution of the trematode Bunodera luciopercae (Muller) in the intestines of juvenile perch infected with plerocercoids of Triaenophorus nodulosus (Pallas). Inland Water Biology 7, 167–171.Google Scholar
Johnson, PTJ, Koprivnikar, J, Orlofske, SA, Melbourne, BA and Lafonte, BE (2014) Making the right choice: testing the drivers of asymmetric infections within hosts and their consequences for pathology. Oikos 123, 875–885.Google Scholar
Kennedy, CR (1974) A checklist of British and Irish freshwater fish parasites with notes on their distribution. Journal of Fish Biology 6, 613–644.Google Scholar
Kennedy, CR, Shears, PC and Shears, JA (2001) Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123, 257–269.Google Scholar
Loot, G, Brosse, S, Lek, S and Guégan, J-F (2001) Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. Freshwater Biology 46, 1219–1227.Google Scholar
Markov, GS and Kosareva, NA (1962) The regular, separate, and joint occurrence of components in fish parasitocoenoses. Zoologicheskii Zhurnal 41, 1477–1487 (in Russian, English translation – British Library Russian Translating Programme, RTS 2392).Google Scholar
Morley, NJ and Lewis, JW (2017) Influence of Triaenophorus nodulosus plerocercoids (Cestoda: Pseudophyllidea) on the occurrence of intestinal helminths in the perch (Perca fluviatilis). Journal of Helminthology 91, 711–717.Google Scholar
Poulin, R (2001) Interactions between species and the structure of helminth communities. Parasitology 122, S3–S11.Google Scholar
Rau, ME, Gordon, DM and Curtis, MA (1979) Bilateral asymmetry of Diplostomum infections in the eyes of lake whitefish Coregonus chipeaformis (Mitchell) and a computer simulation of the observed metacercarial distribution. Journal of Fish Diseases 2, 291–297.Google Scholar
Reiczigel, J and Rozsa, L (2005) Quantitative parasitology 3.0. Budapest, distributed by the authors.Google Scholar
Scholz, T and Kuchta, R (2016) Fish-borne, zoonotic cestodes (Diphyllobothrium and relatives) in cold climates: a never-ending story of neglected and (re)-emergent parasites. Food and Waterborne Parasitology 4, 23–38.Google Scholar
Shigin, AA (1964) The life span of Diplostomum spathaceum in the intermediate host. Trudy Gel'mintologicheskoi Laboratorii Akademiya Nauk SSSR 14, 262–272 (in Russian).Google Scholar
Sweeting, RA (1977) Studies on Ligula intestinalis – some aspects of the pathology in the second intermediate host. Journal of Fish Biology 10, 43–50.Google Scholar
Wayland, MT and Chubb, JC (2016) A new R package and web application for detecting bilateral asymmetry in parasitic infections. Folia Parasitologica 63, 039.Google Scholar
Williams, H and Jones, A (1994) Parasitic worms of fish. London, Taylor & Francis.Google Scholar
Zhokhov, AE and Pugacheva, MN (2012) Distribution and occurrence of Ligula intestinalis (L.) plerocercoids (Cestoda, Ligulidae) in the fishes of Lake Tana, Ethiopia. Inland Water Biology 5, 293–298.Google Scholar