Folia Parasitologica 68:007 (2021) | DOI: 10.14411/fp.2021.007

Molecular and morphological characterisation of the metacercariae of two species of Cardiocephaloides (Digenea: Strigeidae) infecting endemic South African klipfish (Perciformes: Clinidae)

Anja Vermaak1, Nico J. Smit1, Olena Kudlai1,2,3
1 Water Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa;
2 Institute of Ecology, Nature Research Centre, Vilnius, Lithuania;
3 Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic

South African clinids are a major component of the temperate intertidal regions that are also known to participate in life cycles and transmission of several groups of parasites. However, the knowledge of trematode diversity of these fishes is incomplete. In this study, two species of Clinus Cuvier, the super klipfish Clinus superciliosus (Linnaeus) and the bluntnose klipfish Clinus cottoides Valenciennes, were collected from six localities along the South African coast and examined for the presence of trematodes. Metacercariae of Cardiocephaloides Sudarikov, 1959 were found in the eye vitreous humour and brain of C. superciliosus and in the eye vitreous humour of C. cottoides. Detailed analyses integrating morphological and molecular sequence data (28S rDNA, ITS2 rDNA-region, and COI mtDNA) revealed that these belong to two species, Cardiocephaloides physalis (Lutz, 1926) and an unknown species of Cardiocephaloides. This study provides the first report of clinid fishes serving as intermediate hosts for trematodes, reveals that the diversity of Cardiocephaloides in South Africa is higher than previously recorded, and highlights the need for further research to elucidate the life cycles of these trematode species. The broad geographical distribution of Cardiocephaloides spp. was confirmed in the present study based on molecular sequence data. The host-parasite interactions between clinid fishes and metacercariae of Cardiocephaloides are yet to be explored.

Keywords: Trematoda, Clinus superciliosus, Clinus cottoides, marine fish parasites, DNA, morphology

Received: August 12, 2020; Revised: November 18, 2020; Accepted: November 23, 2020; Published online: April 9, 2021  Show citation

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Vermaak, A., Smit, N.J., & Kudlai, O. (2021). Molecular and morphological characterisation of the metacercariae of two species of Cardiocephaloides (Digenea: Strigeidae) infecting endemic South African klipfish (Perciformes: Clinidae). Folia Parasitologica, 68, Article 2021.007. https://doi.org/10.14411/fp.2021.007
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    References

    1. Achatz T.J., Pullis E.E., González-Acuña D., Tkach, V.V. 2020: Phylogenetic relationships of Cardiocephaloides spp. (Digenea, Diplostomoidea) and the genetic characterization of Cardiocephaloides physalis from Magellanic penguin, Spheniscus magellanicus, in Chile. Acta Parasitol. 65: 525‒534. Go to original source... Go to PubMed...
    2. Barnard K.H. 1955: Additions to the Fauna-list of South African Crustacea and Pycnogonida. Ann. S. Afr. Mus. 43: 1‒107
    3. Bartoąová-Sojková P., Kodádková A., Pecková H., Kuchta R., Reed, C.C. 2015: Morphology and phylogeny of two new species of Sphaeromyxa Thélohan, 1892 (Cnidaria: Myxozoa) from marine fish (Clinidae and Trachichthyidae). Parasitology 142: 660‒674. Go to original source... Go to PubMed...
    4. Bartoąová-Sojková P., Lövy A., Reed C.C., Lisnerová M., Tomková T., Holzer A.S., Fiala I. 2018: Life in a rock pool: Radiation and population genetics of myxozoan parasites in hosts inhabiting restricted spaces. PLoS ONE 13: e0194042. Go to original source... Go to PubMed...
    5. Bennett B., Griffiths C.L., Penrith M. 1983: The diets of littoral fish from the Cape Peninsula. South Afr. J. Zool. 18: 343‒352. Go to original source...
    6. Blasco-Costa I., Cutmore S.C., Miller T.L. Nolan M.J. 2016: Molecular approaches to trematode systematics: 'best practice' and implication for future studies. Syst. Parasitol. 93: 295‒306. Go to original source... Go to PubMed...
    7. Born-Torrijos A., Poulin R., Pérez-del-Olmo A., Culurgioni J., Raga J.A., Holzer A.S. 2016: An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds. Int. J. Parasitol. 46: 745‒753. Go to original source... Go to PubMed...
    8. Branch G.M., Griffiths C.L., Branch M.L., Beckley L.E. 2007: Two Oceans: A Guide to the Marine Life of Southern Africa. Struik Publishers, Cape Town, 360 pp.
    9. Brandaõ M., Luque J.L., Scholz T., Kostadinova A. 2013: New records and descriptions of digeneans from the Magellanic penguin Spheniscus magellanicus (Forster) (Aves: Sphenisciformes) on the coast of Brazil. Syst. Parasitol. 85: 79‒98. Go to original source... Go to PubMed...
    10. Bray R.A. 1987: Some helminth parasites of marine fishes of South Africa: family Opecoelidae (Digenea). J. Nat. Hist. 21: 1049‒1075. Go to original source...
    11. Brown A.C. 1982: The biology of sandy-beach whelks of the genus Bullia (Nassariidae). Oceanogr. Mar. Biol. Ann. Rev. 20: 309-361.
    12. Cribb T.H., Anderson G.R., Adlard R.D., Bray R.A. 1998: A DNA-based demonstration of a three-host lifecycle for the Bivesiculidae (Platyhelminthes: Digenea). Int. J. Parasitol. 28: 1791‒1795. Go to original source... Go to PubMed...
    13. Cribb T.H., Bray R.A. 2010: Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Syst. Parasitol. 76: 1‒7. Go to original source... Go to PubMed...
    14. Darriba D., Taboada G.L., Doallo R., Posada D. 2012: jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9: 772. Go to original source... Go to PubMed...
    15. Davies A.J., Smit N.J. 2001: The life cycle of Haemogregarina bigemina (Adeleina: Haemogregarinidae) in South African hosts. Folia Parasitol. 48: 169‒177. Go to original source... Go to PubMed...
    16. Donald K., Spencer H. 2016: Host and ecology both play a role in shaping distribution of digenean parasites of New Zealand whelks (Gastropoda: Buccinidae: Cominella). Parasitology 143: 1143-1156. Go to original source... Go to PubMed...
    17. Dubois G. 1937: Sur quelques Strigéidés. Rev. Suisse Zool. 44: 391‒396. Go to original source...
    18. Dubois G. 1938: Monographie des Strigeida (Trematoda). Mém. Soc. Neuchâtel. Sci. Nat. 6: 1‒535.
    19. Dubois G., Angel M. 1972: Strigeata (Trematoda) of Australian birds and mammals from the Helminthological collection of the University of Adelaide. Trans. R. Soc. S. Aust. 96: 197-215.
    20. Edgar R.C. 2004: MUSCLE: multiple sequence alignment with high accuracy and high throughout. Nucl. Acids Res. 32: 1792‒1797. Go to original source... Go to PubMed...
    21. Espinaze M.P.A., Hui C., Waller L., Dreyer F., Matthee S. 2019: Parasite diversity associated with African penguins (Spheniscus demersus) and the effect of host and environmental factors. Parasitology 146: 791‒804. Go to original source... Go to PubMed...
    22. Fantham H.B. 1919: Some parasitic Protozoa found in South Africa ‒ II. S. Afr. J. Sci. 16: 185‒191.
    23. Fantham H.B. 1930: Some parasitic Protozoa found in South Africa ‒ XIII. S. Afr. J. Sci. 27: 376‒390.
    24. Fishelson L., Gon O., Holdengreber V., Delarea Y. 2007: Comparative spermatogenesis, spermatocytogenesis, and spermatozeugmata formation in males of viviparous species of clinid fishes (Teleostei: Clinidae, Blennioidei). Anat. Rec. 290: 311‒323. Go to original source... Go to PubMed...
    25. Fishelson L., Gon O. 2009: Comparison of the ovaries and oogenesis of some Australian and South African viviparid clinid fishes (Clinidae, Blennioidei, Perciformes). Environ. Biol. Fish. 86: 527‒540. Go to original source...
    26. Gaglio D., Cook T.R., McInnes A., Sherley R.B., Ryan P.G. 2018: Foraging plasticity in seabirds: a non-invasive study of the diet of greater crested terns breeding in the Benguela region. PLoS ONE 13: e0190444. Go to original source... Go to PubMed...
    27. Galaktionov K.V., Dobrovolskij A.A. 2003: The Biology and Evolution of Trematodes. Kluwer Academic Publishing, Dordrecht, London and Boston, 592 pp. Go to original source...
    28. Galazzo D.E., Dayanandan S., Marcogliese D.J., McLauglin J.D. 2002: Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Can. J. Zool. 80: 2207‒2217. Go to original source...
    29. Gon O., Fishelson L., Delarea Y. 2007: Comparative morphology of the oropharyngeal cavity of clinid fish (Perciformes: Clinidae), with particular attention to the form, number and distribution of taste buds, and dentition. Afr. J. Mar. Sci. 29: 283‒298. Go to original source...
    30. Gordy M.A., Hanington P.C. 2019: A fine-scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity. Ecol. Evol. 9: 3153‒3238. Go to original source... Go to PubMed...
    31. Hayes P.M., Lawton S.P., Smit N.J., Gibson W.C., Davies A.J. 2014: Morphological and molecular characterization of a marine fish trypanosome from South Africa, including its development in a leech vector. Parasit. Vector. 7: 50. Go to original source... Go to PubMed...
    32. Hayes P.M., Smit N.J., Seddon A.M., Wertheim D.F., Davies A.J. 2006: A new fish haemogregarine from South Africa and its suspected dual transmission with trypanosomes by a marine leech. Folia Parasitol. 53: 241‒248. Go to original source... Go to PubMed...
    33. Hernández-Mena D.I., García-Prieto L., García-Varela M. 2014: Morphological and molecular differentiation of Parastrigea (Trematoda: Strigeidae) from Mexico, with the description of a new species. Parasitol. Int. 63: 315‒323. Go to original source... Go to PubMed...
    34. Hernández-Mena D.I., García-Varela M., Pérez-Ponce de León G.P. 2017: Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Syst. Parasitol. 94: 833‒848. Go to original source... Go to PubMed...
    35. Holleman W., Von der Heyden S., Zsilavecz G. 2012: Delineating the fishes of the Clinus superciliosus species complex in southern African waters (Blennioidei: Clinidae: Clinini), with the validation of Clinus arborescens Gilchrist & Thompson, 1908 and Clinus ornatus Gilchrist & Thompson, 1908, and with descriptions of two new species. Zool. J. Linn. Soc. 166: 827‒853. Go to original source...
    36. Hoogendoorn C., Smit N.J., Kudlai O. 2020: Resolution of the identity of three species of Diplostomum (Digenea: Diplostomidae) parasitising freshwater fishes in South Africa, combining molecular and morphological evidence. Int. J. Parasitol. Parasites Wildl. 11: 50‒61. Go to original source... Go to PubMed...
    37. Horne E.C., Bray R.A., Bousfield B. 2011: The presence of the trematodes Cardiocephaloides physalis and Renicola sloanei in the African Penguin Spheniscus demersus on the east coast of South Africa. Ostrich 82: 157‒160. Go to original source...
    38. Kensley B., Grindley J.R. 1973: South African parasitic Copepoda. Ann. S. Afr. Mus. 62: 69‒129.
    39. Kudlai O., Cutmore S.C., Cribb T.H. 2015: Morphological and molecular data for three species of the Microphallidae (Trematoda: Digenea) in Australia, including the first descriptions of the cercariae of Maritrema brevisacciferum Shimazu et Pearson, 1991 and Microphallus minutus Johnston, 1948. Folia Parasitol. 62: 053. Go to original source... Go to PubMed...
    40. Kudlai O., Oros M., Kostadinova A., Georgieva S. 2017: Exploring the diversity of Diplostomum (Digenea: Diplostomidae) in fishes from the River Danube using mitochondrial DNA barcodes. Parasit. Vector. 10: 592. Go to original source... Go to PubMed...
    41. Littlewood D.T.J., Curini-Galletti M., Herniou E.A. 2000: The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol. Phylogenetics Evol. 16: 449‒466. Go to original source... Go to PubMed...
    42. Locke S.A., van Dam A., Caffara M., Pinto H.A., Lópex-Hernández D., Blanar C. 2018: Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenetic analysis. Int. J. Parasitol. 48: 1043‒1059. Go to original source... Go to PubMed...
    43. Lutz A. 1926: Strigea physalis, n. sp., parasite de Spheniscus magellanicus (avec démonstration des parasites in situ et sur les préparations). C. R. Séances Soc. Biol. 96: 475‒476.
    44. Morgan J.A.T., Blair D. 1995: Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111: 609‒615. Go to original source... Go to PubMed...
    45. Niewiadomska K. 2002: Family Strigeidae Railliet, 1919. In: D.I. Gibson, A. Jones R.A. Bray (Eds.), Keys to the Trematoda, Volume 1. CAB International, Wallingford, and The Natural History Museum, London, pp. 231-241. Go to original source...
    46. Osset E.A., Fernández M., Raga J.A., Kostadinova A. 2005: Mediterranean Diplodus annularis (Teleostei: Sparidae) and its brain parasite: unforeseen outcome. Parasitol. Int. 54: 201-206. Go to original source... Go to PubMed...
    47. Parukhin A.M. 1968: [Helminth fauna of fishes of South Atlantic.] Biologiya Morya 14: 96‒113. (In Russian.)
    48. Parukhin A.M. 1975: [Special features of the helminth fauna of Clupeiformes in Southern Seas.] Trudy Biologo-Pochvennogo Instituta, Novaya Seriya 26: 143-151. (In Russian.)
    49. Pérez-del-Olmo A., Georgieva S., Pula H.J., Kostadinova A. 2014: Molecular and morphological evidence for three species of Diplostomum (Digenea: Diplostomidae), parasites of fishes and fish-eating birds in Spain. Parasit. Vector. 7: 502. Go to original source...
    50. Perissinotto R., Miranda N.A.F., Raw J.L., Peer N. 2014: Biodiversity census of Lake St Lucia, iSimangaliso Wetland Park (South Africa): gastropod molluscs. Zookeys 440: 1-43. Go to original source...
    51. Prévot G., Bartoli P. 1980: Demonstration of existence of a marine cycle in the strigeids: Cardiocephalus longicollis Szidat, 1928 (Trematoda: Strigeidae). Ann. Parasitol. Hum. Comp. 55: 407‒425. Go to original source... Go to PubMed...
    52. Rambaut A., Suchard M.A., Xie D., Drummond A.J. 2012: FigTree v1.4.3. Available from: http://tree.bio.ed.ac.uk/software.figtree. Accessed 24 February 2020.
    53. Randall R.M., Bray R.A. 1983: Mortalities of jackass penguin Spheniscus demersus chicks caused by trematodes worms Cardiocephaloides physalis. South Afr. J. Zool. 8: 45‒46. Go to original source...
    54. Reed C., MacKenzie K., van der Lingen C.D. 2012: Parasites of South African sardines, Sardinops sagax, and an assessment of their potential as biological tags. Bull. Eur. Assoc. Fish Pathol. 32: 41‒48.
    55. Reed C.C., Basson L., Van As L.L., Dyková I. 2007: Four new myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along the south coast of Africa. Folia Parasitol. 54: 283‒292. Go to original source... Go to PubMed...
    56. Rozas J., Sanchez-DelBarrio J.C., Messeguer X., Rozas R. 2003: DnaSP, DNA polymorphism analyses by thecoalescent and other methods. Bioinformatics 19: 2496-2497. Go to original source... Go to PubMed...
    57. Shigin A.A. 1986: [Trematode Fauna of the USSR. Genus Diplostomum. Metacercariae.] Nauka, Moscow, 253 pp. (In Russian.)
    58. Smit N.J., Davies A.J. 1999: New host records for Haemogregarina bigemina from the coast of southern Africa. J. Mar. Biol. Assoc. U.K. 79: 933‒935. Go to original source...
    59. Snyder S.D., Tkach V.V. 2001: Phylogenetic and biogeographical relationships among some Holarctic frog lung flukes (Digenea: Haematoloechidae). J. Parasitol. 87: 1433‒1440. Go to original source... Go to PubMed...
    60. Timi J.T., Martorelli S.R., Sardella N.H. 1999: Digenetic trematodes parasitic on Engraulis anchoita (Pisces: Engraulidae) from Argentina and Uruguay. Folia Parasitol. 46: 132‒138.
    61. Tkach V.V., Littlewood D.T.J., Olson P.D., Kinsella J.M., Swiderski Z. 2003: Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst. Parasitol. 56: 1‒15. Go to original source... Go to PubMed...
    62. Tkach V.V., Snyder S.D., Swiderski Z. 2001: On the phylogenetic relationship of some members of Macroderoididae and Ochetosomatidae (Digenea, Plagiorchioidea). Acta Parasitol. 46: 267‒275.
    63. Ukomadu N.M. 2017: Assessment of the population structure of the South African sardine Sardinops sagax using a multi-method approach and morphological and molecular characterization of a stock discriminating digenean parasite biotag of the genus Cardiocephaloides. PhD thesis, University of Cape Town, 267 pp.
    64. Van Steenkiste N., Locke S.A., Castelin M., Marcogliese D.J., Abbott C.L. 2015: New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Mol. Ecol. Resour. 15: 945‒952. Go to original source... Go to PubMed...
    65. Von der Heyden S., Bowie R.C.K., Prochazka K., Bloomers P., Crane N.L., Bernardi G. 2011: Phylogeographic patterns and cryptic speciation across oceanographic barriers in South African intertidal fishes. J. Evol. Biol. 24: 2505‒2519. Go to original source... Go to PubMed...
    66. van der Wal S., Smit N.J., Hadfield K.A. 2019: Review of the fish parasitic genus Elthusa Schioedte & Meinert, 1884 (Crustacea, Isopoda, Cymothoidae) from South Africa, including the description of three new species. Zookeys 841: 1‒37. Go to original source... Go to PubMed...
    67. Weston L.F., Reed C.C., Hendricks M., Winker H., van der Lingen C.D. 2015: Stock discrimination of South African sardine (Sardinops sagax) using a digenean parasite biological tag. Fish. Res. 164: 120‒129. Go to original source...

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