Folia Parasitologica 69:018 (2022) | DOI: 10.14411/fp.2022.018

Different hosts in different lakes: prevalence and population genetic structure of plerocercoids of Ligula intestinalis (Cestoda) in Czech water bodies

Masoud Nazarizadeh1, 2, Jiří Peterka3, Jan Kubečka3, Mojmír Vašek3, Tomáš Jůza3, Karlos Ribeiro de Moraes3, Martin Čech3, Michaela Holubová3, Allan T. Souza3, Petr Blabolil2, 3, Milan Muška3, Lobsang Tsering3, Daniel Bartoň3, Milan Říha3, Marek Šmejkal3, Michal Tušer3, Lukáš Vejřík3, Jaroslava Frouzová3, Ivan Jarić3, Marie Prchalová3, Ivana Vejříková3, Jan Štefka ORCID...1, 2*
1 Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic;
2 Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic;
3 Institute of Hydrobiology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic

Ligula intestinalis (Linnaeus, 1758) is a tapeworm parasite with a worldwide distribution that uses a wide variety of fish species as its second intermediate host. In the present study, we investigated the prevalence and population genetic structure of plerocercoids of L. intestinalis in five common cyprinoid species, roach Rutilus rutilus (Linnaeus), freshwater bream Abramis brama (Linnaeus), white bream Blicca bjoerkna (Linnaeus), bleak Alburnus alburnus (Linnaeus), and rudd Scardinius erythrophthalmus (Linnaeus), collected in six water bodies of the Czech Republic (Milada, Most, Medard, Jordán, Římov and Lipno). Of the six study sites, the highest frequency of parasitism was recorded in Lake Medard (15%). The overall prevalence rate among the species was as follows: roach > rudd ≥ freshwater bream > bleak > white bream. Two mitochondrial genes (cytb and COI) were used to compare the population genetic structure of parasite populations using selected samples from the five fish species. The results of the phylogenetic analysis indicated that all populations of L. intestinalis were placed in Clade A, previously identified as the most common in Europe. At a finer scale, haplotype network and PCoA analyses indicated the possible emergence of host specificity of several mtDNA haplotypes to the freshwater bream. Moreover, pairwise Fixation indices (FST) revealed a significant genetic structure between the parasite population in freshwater bream and other host species. Parasite populations in roach not only showed the highest rate of prevalence but also depicted a maximum number of shared haplotypes with populations from bleak and rudd. Our results suggest that recent ecological differentiation might have influenced tapeworm populations at a fine evolutionary scale. Thus, the differences in prevalence between fish host species in different lakes might be influenced not only by the parasite's ecology, but also by its genetic diversity.

Keywords: tapeworm, Czech Republic, host specificity, freshwater, fish parasite

Received: October 29, 2021; Revised: April 20, 2022; Accepted: April 26, 2022; Published online: September 15, 2022  Show citation

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Nazarizadeh, M., Peterka, J., Kubečka, J., Vašek, M., Jůza, T., de Moraes, K.R., ... Štefka, J. (2022). Different hosts in different lakes: prevalence and population genetic structure of plerocercoids of Ligula intestinalis (Cestoda) in Czech water bodies. Folia Parasitologica69, Article 2022.018. https://doi.org/10.14411/fp.2022.018
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References

  1. Appelberg M., Berger H.-M., Hesthagen T., Kleiven E., Kurkilahti M., Raitaniemi J., Rask M. 1995: Development and intercalibration of methods in Nordic freshwater fish monitoring. Water. Air. Soil Pollut. 85: 401-406. Go to original source...
  2. Arme C., Owen R.W. 1968: Occurrence and pathology of Ligula intestinalis infections in British fishes. J. Parasitol. 54: 272-280. Go to original source... Go to PubMed...
  3. Barson M., Marshall B.E. 2003: The occurrence of the tapeworm Ligula intestinalis (L.), in Barbus paludinosus from a small dam in Zimbabwe. African J. Aquat. Sci. 28: 175-178. Go to original source...
  4. Baruš V., Prokeš M. 1995: Length-weight relationship of Ligula intestinalis plerocercoids in adult silver bream and discussion on estimation of the parasite age. Appl. Parasitol. 36: 192-199. Go to PubMed...
  5. Bean C.W., Winfield I.J. 1991: Influences of the tapeworm Ligula intestinalis (L.) on the spatial distributions of juvenile roach Rutilus rutilus (L.) and gudgeon Gobio gobio (L.) in Lough Neagh, Northern Ireland. Netherlands J. Zool.42: 419-429. Go to original source...
  6. Bernard M.S., Strittmatter M., Murúa P., Heesch S., Cho G.Y., Leblanc C., Peters A.F. 2019: Diversity, biogeography and host specificity of kelp endophytes with a focus on the genera Laminarionema and Laminariocolax (Ectocarpales, Phaeophyceae). Eur. J. Phycol. 54: 39-51. Go to original source...
  7. Blabolil P., Boukal D.S., Ricard D., Kubečka J., Říha M., Vašek M., Prchalová M., Čech M., Frouzová J., Jůza T., Muška M., Tušer M., Draštík V., Šmejkal M., Vejřík L., Peterka J. 2017: Optimal gillnet sampling design for the estimation of fish community indicators in heterogeneous freshwater ecosystems. Ecol. Indic. 77: 368-376. Go to original source...
  8. Blatrix R., Herbers J.M. 2003: Coevolution between slave-making ants and their hosts: host specificity and geographical variation. Mol. Ecol. 12: 2809-2816. Go to original source... Go to PubMed...
  9. Blouin M.S. 2002: Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int. J. Parasitol. 32: 527-531. Go to original source... Go to PubMed...
  10. Bouzid W., Lek S., Mace M., Ben Hassine O., Etienne R., Legal L., Loot G. 2008a: Genetic diversity of Ligula intestinalis (Cestoda: Diphyllobothriidea) based on analysis of inter-simple sequence repeat markers. J. Zool. Syst. Evol. Res. 46: 289-296. Go to original source...
  11. Bouzid W., Štefka J., Bahri-Sfar L., Beerli P., Loot G., Lek S., Haddaoui N., Hypša V., Scholz T., Dkhil-Abbes T. 2013: Pathways of cryptic invasion in a fish parasite traced using coalescent analysis and epidemiological survey. Biol. Invasions 15: 1907-1923. Go to original source...
  12. Bouzid W., Štefka J., Hypša V., Lek S., Scholz T., Legal L., Hassine O.K. Ben, Loot G. 2008b: Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). Int. J. Parasitol. 38: 1465-1479. Go to original source... Go to PubMed...
  13. Britton J.R., Jackson M.C., Harper D.M. 2009: Ligula intestinalis (Cestoda: Diphyllobothriidae) in Kenya: a field investigation into host specificity and behavioural alterations. Parasitology 136: 1367-1373. Go to original source... Go to PubMed...
  14. Brown S.P., Loot G., Grenfell B.T., Guégan J.F. 2001: Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123: 519. Go to original source... Go to PubMed...
  15. Bykhovskaya-Pavlovskaya I.E. 1964: Key to Parasites of Freshwater Fish of the USSR. Israel Program for Scientific Translations, Jerusalem, 919 pp.
  16. Carter B.C., Shubeita G.T., Gross S.P. 2005: Tracking single particles: a user-friendly quantitative evaluation. Phys. Biol. 2: 60. Go to original source... Go to PubMed...
  17. Chapman A., Hobbs R.P., Morgan D.L., Gill H.S. 2006: Helminth parasitism of Galaxias maculatus (Jenyns, 1842) in southwestern Australia. Ecol. Freshw. Fish. 15: 559-564. Go to original source...
  18. Cole R., Viney M. 2019: Correction to: The population genetics of parasitic nematodes of wild animals. Parasit. Vectors. 12: 1. Go to original source... Go to PubMed...
  19. Dence W.A. 1958: Studies on Ligula-infected common shiners (Notropis cornutus frontalis Agassiz) in the Adirondacks. J. Parasitol 44: 334-338. Go to original source... Go to PubMed...
  20. Dubinina M.N. 1980: Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. Amerind Publishing Company, Delhi, 320 pp.
  21. Ergonul M.B., Altindag A. 2005: The occurrence and dynamics of Ligula intestinalis in its cyprinid fish host, tench, Tinca tinca, in Mogan Lake (Ankara, Turkey). Vet. Med. 50: 537. Go to original source...
  22. Groves K.L., Shields B.A. 2001: Observations on the plerocercoid stage of the tapeworm Ligula in three species of fish from the lower Crooked River of central Oregon. J. Aquat. Anim. Health. 13: 285-289. Go to original source...
  23. Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S. 2018: UFBoot2: Improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35: 518-522. Go to original source... Go to PubMed...
  24. Holmes J.C., Bethel W.M. 1972: Modification of intermediate host behavior by parasites. In: E.U. Canning and C.A. Wright (Eds.), Behavioral Aspects of Parasite Transmission, Academic Press, New York, pp. 128-149.
  25. Huyse T., Poulin R., Théron A., Theron A. 2005: Speciation in parasites: a population genetics approach. Trends Parasitol. 21: 469-475. Go to original source... Go to PubMed...
  26. Ivankov V.N., Kaplunenko V.A., Bol'shakov S.G., Zheleznova L. V. 2020: First detections of the tapeworm Ligula intestinalis (Linnaeus, 1758) (Cestoda: Ligulidae) in the anadromous far eastern redfin Tribolodon hakonensis (Gunther, 1880) (Teleostei: Cyprinidae) in Primorye. Russ. J. Mar. Biol. 46: 230-231. Go to original source...
  27. Iwanowicz D.D. 2011: Overview on the effects of parasites on fish health. In: R.C. Cipriano, A.W. Bruckner and I.S. Shchelkunov (Eds.), Proceedings of the Third Bilateral Conference between Russia and the United States, Aquatic Animal Health 2009, Shepherdstown, 12-20 July 2009. Khaled bin Sultan Living Oceans Foundation, Landover, pp. 176-184.
  28. Jombart T. 2008: adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405. Go to original source... Go to PubMed...
  29. Kennedy C.R. 1974: A checklist of British and Irish freshwater fish parasites with notes on their distribution. J. Fish Biol. 6: 613-644. Go to original source...
  30. Kennedy C.R., Burrough R.J. 1981: The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis (L.). J. Fish Biol. 19: 105-126. Go to original source...
  31. Kennedy C.R., Shears P.C., Shears J.A. 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. Go to original source... Go to PubMed...
  32. Kočová P. 2018: [Population-genomic analysis of adaptation in a parasite with a wide host range - tapeworm Ligula intestinalis.] Master thesis, University of South Bohemia in České Budějovice. (In Czech.)
  33. Lagrue C., Presswell B., Dunckley N., Poulin R. 2018: The invasive cestode parasite Ligula from salmonids and bullies on the South Island, New Zealand. Parasitol. Res. 117: 151-156. Go to original source... Go to PubMed...
  34. Lanfear R., Frandsen P.B., Wright A.M., Senfeld T., Calcott B. 2017: Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34: 772-773. Go to original source... Go to PubMed...
  35. Leigh J.W., Bryant D. 2015: POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6: 1110-1116. Go to original source...
  36. Levron C., Sitko J., Scholz T. 2009: Spermiogenesis and spermatozoon of the tapeworm Ligula intestinalis (Diphyllobothriidea): phylogenetic implications. J. Parasitol. 95: 1-9. Go to original source... Go to PubMed...
  37. Li J., Liao X., Yang H. 2000: Molecular characterization of a parasitic tapeworm (Ligula) based on DNA sequences from formalin-fixed specimens. Biochem. Genet. 38: 309-322. Go to original source... Go to PubMed...
  38. Librado P., Rozas J. 2009: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452. Go to original source... Go to PubMed...
  39. Longshaw M., Frear P.A., Nunn A.D., Cowx I.G., Feist S.W. 2010: The influence of parasitism on fish population success. Fish. Manag. Ecol. 17: 426-434. Go to original source...
  40. Loot G., Francisco P., Santoul F., Lek S., Guégan J.-F. 2001: The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France. Arch. Hydrobiol. 152: 511-525. Go to original source...
  41. Martinů J., Hypša V., Štefka J. 2018: Host specificity driving genetic structure and diversity in ectoparasite populations: coevolutionary patterns in Apodemus mice and their lice. Ecol. Evol. 8: 10008-10022. Go to original source... Go to PubMed...
  42. Meinilä M., Kuusela J., Ziętara M.S., Lumme J. 2004: Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). Int. J. Parasitol. 34: 515-526. Go to original source... Go to PubMed...
  43. Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., von Haeseler A., Lanfear R. 2020: IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37: 1530-1534. Go to original source... Go to PubMed...
  44. Ministry of Agriculture of the Czech Republic 2019: Report on Water Management in the Czech Republic in 2019, Accessed April 25, 2022, https://eagri.cz/Report
  45. Moravec F., Scholz T. 2016: Helminth parasites of the lesser great cormorant Phalacrocorax carbo sinensis from two nesting regions in the Czech Republic. Folia Parasitol. 63: 022. Go to original source... Go to PubMed...
  46. Morgan D.L. 2003: Distribution and biology of Galaxias truttaceus (Galaxiidae) in south-western Australia, including first evidence of parasitism of fishes in Western Australia by Ligula intestinalis (Cestoda). Environ. BioL. Fishes. 66:155-167. Go to original source...
  47. Nazarizadeh M., Martinů J., Nováková M., Stanko M., Štefka J. 2022: Phylogeography of the parasitic mite Laelaps agilis in Western Palearctic shows lineages lacking host specificity but possessing different demographic histories. BMC Zool. 7: 15. Go to original source... Go to PubMed...
  48. Nezafat R.B., Khara H., Satari M. 2008: Parasite infection of bream (Abramis brama orientalis Berg, 1949) in Aras Dam lake. J. Biol. Sci. 2: 83-96.
  49. Nosil P. 2012: Ecological Speciation. Oxford University Press, Oxford, 280 pp. Go to original source...
  50. Olson P.D., Littlewood D.T.J., Griffiths D., Kennedy C.R., Arme C. 2002: Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. J. Helminthol. 76: 171. Go to original source... Go to PubMed...
  51. Palm H.W., Theisen S., Pikalov E., Kleinertz S. 2018: An update: manipulation of fish phenotype by parasites. Ref. Mod. Life Sci. 2018: 1-9. Go to original source...
  52. R Core Team 2021: R: a language and environment for statistical computing.
  53. Ristau K., Steinfartz S., Traunspurger W. 2013: First evidence of cryptic species diversity and significant population structure in a widespread freshwater nematode morphospecies (Tobrilus gracilis). Mol. Ecol. 22: 4562-4575. Go to original source... Go to PubMed...
  54. Ronquist F., Huelsenbeck J.P. 2003: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. Go to original source... Go to PubMed...
  55. Rundle H.D., Nosil P. 2005: Ecological speciation. Ecol. Lett. 8: 336-352. Go to original source...
  56. Ryšavý B., Sitko J. 1995: New findings of tapeworms (Cestoda) of birds from Moravia and synopsis of bird Cestodes from Czech Republic. Acta Sci. Nat. Brno 29: 1-66.
  57. Schirrmann M.K., Leuchtmann A. 2015: The role of host-specificity in the reproductive isolation of Epichloë endophytes revealed by reciprocal infections. Fungal Ecol. 15: 29-38. Go to original source...
  58. Štefka J., Hypša V., Scholz T. 2009: Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Mol. Ecol. 18: 1187-1206. Go to original source... Go to PubMed...
  59. Stork N.E., Lyal C.H.C. 1993: Extinction or 'co-extinction' rates? Nature 366: 307. Go to original source...
  60. Sweeting R.A. 1977: Studies on Ligula intestinalis. Some aspects of the pathology in the second intermediate host. J. Fish Biol. 10: 43-50. Go to original source...
  61. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011: MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739. Go to original source... Go to PubMed...
  62. Van Dobben W.H. 1952: The food of the cormorant in the Netherlands. Ardea 55: 1-63. Go to original source...
  63. Waeschenbach A., Brabec J., Scholz T., Littlewood D.T.J., Kuchta R. 2017: The catholic taste of broad tapeworms - multiple routes to human infection. Int. J. Parasitol. 47: 831-843. Go to original source... Go to PubMed...
  64. Wells K., Clark N.J. 2019: Host specificity in variable environments. Trends Parasitol. 35: 452-465. Go to original source... Go to PubMed...
  65. Windsor D.A. 1998: Controversies in parasitology. Most of the species on Earth are parasites. Int. J. Parasitol. 28: 1939-1941. Go to original source... Go to PubMed...
  66. Wyatt R.J., Kennedy C.R. 1989: Host-constrained epidemiology of the fish tapeworm Ligula intestinalis (L.). J. Fish Biol. 35: 215-227. Go to original source...
  67. Xia X., Lemey P. 2009: Assessing substitution saturation with DAMBE. In: P. Lemey, M. Salemi, A.-M. Vandamme (Eds.), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. Second Edition. Cambridge University Press, Cambridge, pp. 615-630. Go to original source...
  68. Xia X., Xie Z. 2001: DAMBE: software package for data analysis in molecular biology and evolution. J. Hered. 92: 371-373. Go to original source... Go to PubMed...
  69. ZAR J.H. 1999: Biostatistical Analysis. Prentice Hall, New Jersey, 663 pp.