Systematic Parasitology

, Volume 89, Issue 2, pp 133–152 | Cite as

Four marine digenean parasites of Austrolittorina spp. (Gastropoda: Littorinidae) in New Zealand: morphological and molecular data

  • Katie O’Dwyer
  • Isabel Blasco-Costa
  • Robert Poulin
  • Anna Faltýnková


Littorinid snails are one particular group of gastropods identified as important intermediate hosts for a wide range of digenean parasite species, at least throughout the Northern Hemisphere. However nothing is known of trematode species infecting these snails in the Southern Hemisphere. This study is the first attempt at cataloguing the digenean parasites infecting littorinids in New Zealand. Examination of over 5,000 individuals of two species of the genus Austrolittorina Rosewater, A. cincta Quoy & Gaimard and A. antipodum Philippi, from intertidal rocky shores, revealed infections with four digenean species representative of a diverse range of families: Philophthalmidae Looss, 1899, Notocotylidae Lühe, 1909, Renicolidae Dollfus, 1939 and Microphallidae Ward, 1901. This paper provides detailed morphological descriptions of the cercariae and intramolluscan stages of these parasites. Furthermore, partial sequences of the 28S rRNA gene and the mitochondrial gene cytochrome c oxidase subunit 1 (cox1) for varying numbers of isolates of each species were obtained. Phylogenetic analyses were carried out at the superfamily level and along with the morphological data were used to infer the generic affiliation of the species.


Ventral Sucker Oral Sucker Cox1 Sequence Cephalic Region Excretory Vesicle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We would like to thank Aneta Kostadinova (Institute of Parasitology, Academy of Sciences of the Czech Republic) for her in-depth guidance and comments and the Linnean Society of New South Wales and the Otago Museum Linneaus Fellowship for funds provided to KoD. This study was partially supported by the Czech Science Foundation (grant P505/12/G112).


  1. Al-Kandari, W. Y., Al-Bustan, S. A., & Alnaqeeb, M. (2011). Ribosomal DNA sequence characterisation of Maritrema cf. eroliae Yamaguti, 1939 (Digenea: Microphallidae) and its life cycle. Journal of Parasitology, 97, 1067–1074.PubMedCrossRefGoogle Scholar
  2. Angel, L. M. (1954). Parorchis acanthus var. australis, n. var., with an account of the life cycle in South Australia. Transactions of the Royal Society of South Australia, 77, 164–174.Google Scholar
  3. Bayssade-Dufour, C. H. (1979). L’appareil sensoriel des cercaires et la systématique des trématodes digénétiques. Memoires du Muséum National d’Histoire Naturelle, Serie A Zoologie, 113, 1–81.Google Scholar
  4. Bisset, S. A. (1977). Notocotylus tadornae n. sp. and Notocotylus gippyensis (Beverley-Burton, 1958) (Trematoda: Notocotylidae) from waterfowl in New Zealand: Morphology, life history and systematic relations. Journal of Helminthology, 51, 365–372.CrossRefGoogle Scholar
  5. Blakeslee, A. M. H., & Byers, J. E. (2008). Using parasites to inform ecological history: Comparisons among three congeneric marine snails. Ecology, 89, 1068–1078.PubMedCrossRefGoogle Scholar
  6. Blasco-Costa, I., Waters, J. M., & Poulin, R. (2012). Swimming against the current: Genetic structure, host mobility and the drift paradox in trematode parasites. Molecular Ecology, 21, 207–217.PubMedCrossRefGoogle Scholar
  7. Bogéa, T. (2004). Functional and phylogenetic components in cercarial nervous systems. Folia Parasitologica, 51, 311–319.PubMedCrossRefGoogle Scholar
  8. Bowles, J., Hope, M., Tiu, W. U., Liu, X., & McManus, D. P. (1993). Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica, 55, 217–229.PubMedCrossRefGoogle Scholar
  9. Boyce, K., Hide, G., Craig, P. S., Harris, P. D., Reynolds, C., Pickles, A., & Rogan, M. T. (2012). Identification of a new species of digenean Notocotylus malhamensis n. sp. (Digenea: Notocotylidae) from the bank vole (Myodes glareolus) and the field vole (Microtus agrestis). Parasitology, 139, 1630–1639.Google Scholar
  10. Cable, R. M. (1963). Marine cercariae from Curaçao and Jamaica. Zeitschrift für Parasitenkunde, 23, 429–469.PubMedGoogle Scholar
  11. Church, M. L., Barrett, P. M., Swenson, J., Kinsella, J. M., & Tkach, V. V. (2013). Outbreak of Philophthalmus gralli in four greater rheas (Rhea americana). Veterinary Ophthalmology, 16, 65–72.PubMedCrossRefGoogle Scholar
  12. Cort, W. W. (1914). Larval trematodes from North American fresh-water snails. Journal of Parasitology, 1, 65–84.CrossRefGoogle Scholar
  13. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9, 772.PubMedCrossRefGoogle Scholar
  14. Davies, M. S., & Williams, G. A. (1998). Aspects of littorinid biology - Epilogue. Hydrobiologia, 378, 243–246.CrossRefGoogle Scholar
  15. Deblock, S. (1980). Inventaire des trématodes larvaires parasites des mollusques Hydrobia (Prosobranches) des côtes de France. Parassitologia, 22, 1–105.PubMedGoogle Scholar
  16. Detwiler, J. T., Zajac, A. M., Minchella, D. J., & Belden, L. K. (2012). Revealing cryptic parasite diversity in a definitive host: Echinostomes in muskrats. Journal of Parasitology, 98, 1148–1155.PubMedCrossRefGoogle Scholar
  17. Galaktionov, K. V., Blasco-Costa, I., & Olson, P. D. (2012). Life cycles, molecular phylogeny and historical biogeography of the “pygmaeus” microphallids (Digenea: Microphallidae): Widespread parasites of marine and coastal birds in the Holarctic. Parasitology, 139, 1346–1360.PubMedCrossRefGoogle Scholar
  18. Galaktionov, K. V., & Skirnísson, K. (2000). Digeneans from intertidal molluscs of SW Iceland. Systematic Parasitology, 47, 87–101.PubMedCrossRefGoogle Scholar
  19. Gilardoni, C., Ituarte, C., & Cremonte, F. (2012). Castrating effects of trematode larvae on the reproductive success of a highly parasitised population of Crepipatella dilatata (Caenogastropoda) in Argentina. Marine Biology, 159, 2259–2267.CrossRefGoogle Scholar
  20. Granovitch, A. I., & Maximovich, A. N. (2013). Long-term population dynamics of Littorina obtusata: The spatial structure and impact of trematodes. Hydrobiologia, 706, 91–101.CrossRefGoogle Scholar
  21. Granovitch, A. I., & Mikhailova, N. A. (2004). Rocky shore trematodes of the west coast of Sweden: Distribution and life cycle strategies. Acta Parasitologica, 49, 228–236.Google Scholar
  22. Griffin, M. J., Khoo, L. H., Quiniou, S. M., O’Hear, M. M., Pote, L. M., Greenway, T. E., & Wise, D. J. (2012). Genetic sequence data identifies the cercaria of Drepanocephalus spathans (Digenea: Echinostomatidae), a parasite of the double-crested cormorant (Phalacrocorax auritus), with notes on its pathology in juvenile channel catfish (Ictalurus punctatus). Journal of Parasitology, 98, 967–972.Google Scholar
  23. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.PubMedCrossRefGoogle Scholar
  24. Hechinger, R. F., & Miura, O. (2014). Two “new” renicolid trematodes (Trematoda: Digenea: Renicolidae) from the California horn snail, Cerithidea californica (Haldeman, 1840) (Gastropoda: Potamididae). Zootaxa, 3784, 559–574.PubMedCrossRefGoogle Scholar
  25. Howell, M. (1965). Notes on a potential trematode parasite of man in New Zealand. Tuatara, 13, 182–183.Google Scholar
  26. James, B. L. (1968). The distribution and keys of species in the Littorinidae and of their digenean parasites in the region of Dale, Pembrokeshire. Field Studies, 2, 615–650.Google Scholar
  27. Kanev, I., Radev, V., & Fried, B. (2005). Family Philophthalmidae Looss, 1899. In: Jones, A., Bray, R. A., & Gibson, D. (Eds) Keys to the Trematoda. Volume 2. Wallingford: CAB International and The Natural History Museum, pp. 87–97.Google Scholar
  28. Katoh, K., & Standley, D. M. (2013). MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution, 30, 772–780.PubMedCentralPubMedCrossRefGoogle Scholar
  29. Keeney, D. B., King, T. M., Rowe, D. L., & Poulin, R. (2009). Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites. Molecular Ecology, 18, 4591–4603.PubMedCrossRefGoogle Scholar
  30. Leung, T. L. F., Donald, K. M., Keeney, D. B., Koehler, A. V., Peoples, R. C., & Poulin, R. (2009). Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: Life cycles, ecological roles and DNA barcodes. New Zealand Journal of Marine and Freshwater Research, 43, 857–865.CrossRefGoogle Scholar
  31. Lockyer, A. E., Olson, P. D., & Littlewood, D. T. J. (2003). Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): Implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–171.CrossRefGoogle Scholar
  32. Lotfy, W. M., Brant, S. V., DeJong, R. J., Le, T. H., Demiaszkiewicz, A., Rajapakse, R. P., Perera, V. B., Laursen, J. R., & Loker, E. S. (2008). Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). American Journal of Tropical Medicine and Hygiene, 79, 248–255.Google Scholar
  33. Martin, W. E. (1956). The life cycle of Catatropis johnstoni n. sp. (Trematoda: Notocotylidae). Transactions of the American Microscopical Society, 75, 117–128.CrossRefGoogle Scholar
  34. Martin, W. E. (1971). Larval stages of renicolid trematodes. Transactions of the American Microscopical Society, 90, 188–194.CrossRefGoogle Scholar
  35. Martorelli, S. R., Fredensborg, B. L., Leung, T. L. F., & Poulin, R. (2008). Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). New Zealand Journal of Zoology, 35, 73–84.CrossRefGoogle Scholar
  36. McKenna, P. (2010). An updated checklist of helminth and protozoan parasites of birds in New Zealand. Webmed Central Parasitology, 1, WMC00705.Google Scholar
  37. Mouritsen, K. N., & Poulin, R. (2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology, 124, S101–S117.PubMedGoogle Scholar
  38. Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A., & Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.PubMedCrossRefGoogle Scholar
  39. Rees, G. (1937). The anatomy and encystment of Cercaria purpurae Lebour, 1911. Proceedings of the Zoological Society of London, B107, 65–73.CrossRefGoogle Scholar
  40. Reid, D. G., & Williams, S. T. (2004). The subfamily Littorininae (Gastropoda: Littorinidae) in the temperate southern hemisphere: The genera Nodilittorina, Austrolittorina and Afrolittorina. Records of the Australian Museum, 56, 75–122.CrossRefGoogle Scholar
  41. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.Google Scholar
  42. Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675.PubMedCrossRefGoogle Scholar
  43. Skirnísson, K., & Galaktionov, K. V. (2002). Life cycles and transmission patterns of seabird digeneans in SW Iceland. Sarsia, 87, 144–151.CrossRefGoogle Scholar
  44. Smith, S. J., & Hickman, J. L. (1983). Two new notocotylid trematodes from birds in Tasmania and their life histories. Papers and Proceedings of the Royal Society of Tasmania, 117, 85–103.Google Scholar
  45. Szabo, M.J. 2013. Spotted shag. In: Miskelly, C. M. (Ed.) New Zealand Birds Online. Last accessed: 08/07/2014.
  46. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.PubMedCrossRefGoogle Scholar
  47. Telford, M. J, Herniou, E. A., Russell, R. B., & Littlewood, D. T. J. (2000). Changes in mitochondrial genetic codes as phylogenetic characters: Two examples from the flatworms. Proceedings of the National Academy of Sciences of the United States of America, 97, 11359–11364.Google Scholar
  48. Thieltges, D. W., Ferguson, M. A. D., Jones, C. S., Noble, L. R., & Poulin, R. (2009). Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe. Journal of Biogeography, 36, 1493–1501.CrossRefGoogle Scholar
  49. Thieltges, D. W, Krakau, M., Andresen, H., Fottner, S., & Reise, K. (2006). Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgoland Marine Research, 60, 307–316.CrossRefGoogle Scholar
  50. 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). Systematic Parasitology, 56, 1–15.PubMedCrossRefGoogle Scholar
  51. Tkach, V., Pawlowski, J., & Mariaux, J. (2000). Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology, 30, 83–93.PubMedCrossRefGoogle Scholar
  52. Tkach, V., Pawlowski, J., Mariaux, J., & Swiderski, Z. (2001). Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: Littlewood, D.T., & Bray, R. A. (Eds) Interrelationships of the Platyhelminthes. London: Taylor & Francis, pp. 186–193.Google Scholar
  53. Unwin, S., Chantrey, J., Chatterton, J., Aldhoun, J. A., & Littlewood, D. T. J. (2013). Renal trematode infection due to Paratanaisia bragai in zoo housed Columbiformes and a red bird-of-paradise (Paradisaea rubra). International Journal for Parasitology: Parasites and Wildlife, 2, 32–41.PubMedCentralPubMedGoogle Scholar
  54. Velasquez, C. C. (1969). Life history of Paramonostomum philippinensis sp. n. (Trematoda: Digenea: Notocotylidae). Journal of Parasitology, 55, 289–292.PubMedCrossRefGoogle Scholar
  55. Werle, E., Schneider, C., Renner, M., Volker, M., & Fiehn, W. (1994). Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research, 22, 4354–4355.PubMedCentralPubMedCrossRefGoogle Scholar
  56. Yamaguti, S. (1975). A synoptical review of life histories of digenetic trematodes of vertebrates with special reference to the morphology of their larval forms. Tokyo: Keigaku Publishing Co., 590 pp.Google Scholar
  57. Zikmundová, J., Georgieva, S., Faltýnková, A., Soldánová, M., & Kostadinova, A. (2014). Species diversity of Plagiorchis Lühe, 1899 (Digenea: Plagiorchiidae) in lymnaeid snails from freshwater ecosystems in central Europe revealed by molecules and morphology. Systematic Parasitology, 88, 37–54.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Katie O’Dwyer
    • 1
  • Isabel Blasco-Costa
    • 1
  • Robert Poulin
    • 1
  • Anna Faltýnková
    • 2
  1. 1.Evolutionary and Ecological Parasitology Group, Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Institute of ParasitologyBiology Centre of the Academy of Sciences of the Czech RepublicČeské BudějovoiceCzech Republic

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