, Volume 706, Issue 1, pp 103–118 | Cite as

Long-term variation in trematode (Trematoda, Digenea) component communities associated with intertidal gastropods is linked to abundance of final hosts

  • Ivan A. Levakin
  • Kirill E. Nikolaev
  • Kirill V. Galaktionov


Trematodes are abundant parasites essential for maintaining stability of marine intertidal ecosystems. Despite the great ecological significance of trematodes, long-term dynamics of their communities remains practically unstudied. This study, based on 12-year-long seasonal monitoring of infection of Littorina and Hydrobia snails with 16 trematode species in the White Sea, aimed to reveal factors determining long-term variation in infection of intertidal snails by trematode parthenitae and larvae. Using the state-of-the-art method of singular spectrum analysis, we revealed trends in this variation and assessed their significance. Interestingly, these trends were not associated with oceanic and climatic parameters but were mostly determined by changes in abundance of the trematode final hosts. Moreover, the prevalence trends turned out to be connected with both large-scale events and local factors at the scale of the intertidal site. The main factors determining the long-term dynamics of the trematode component communities in the study area were the decreasing abundance of birds due to growing anthropogenic disturbance and the increasing abundance of the three-spined stickleback. The analysis of long-term trends of trematode prevalence in intertidal snails may be a sensitive indicator of the abundance dynamics of final hosts in the coastal areas of temperate and northern seas.


Parasitological monitoring Singular spectrum analysis Trematode communities Trematode life cycles Intertidal zone Northern seas 



We are grateful to the foundations that have supported this research over the years: INTAS (the International Association for the Promotion of Co-operation with Scientists from the New Independent States of the Former Soviet Union), RFBR (the Russian Foundation for Basic Research) and St. Petersburg State University (Grant Number We thank Natalia Lentsman for her help with English translation of the MS. We thank the anonymous reviewers for their well-considered comments on an earlier draft of the manuscript.

Supplementary material

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Supplementary material 1 (DOC 88 kb)


  1. Berger, V., A. Naumov, M. Zubaha, N. Usov, I. Smolyar, R. Tatusko & S. Levitus, 2003. 36-Year time series (1963–1998) of zooplankton, temperature and salinity in the White Sea. S-Peterburg–Washington: 362 pp.Google Scholar
  2. Berger, V. J., Naumov, A. D. & A. A. Sukhotin, 2012. Conclusion. Concentration of pollutants in the White Sea organisms. In Berger, V. J. (ed.), Biological Resources of the White Sea and their Rational Exploitation. Explorations of Fauna of the Seas, 69 (77). Zoological Institute of the Russian Academy of Sciences Publishing, St. Petersburg: 320–325 (in Russian).Google Scholar
  3. Bustnes, J. O., K. V. Galaktionov & S. W. B. Irwin, 2000. Potential threats to littoral biodiversity: is increased parasitism a consequence of human activity? Oikos 90: 189–190.CrossRefGoogle Scholar
  4. Byers, J. E., A. M. H. Blakeslee, E. Linder, A. B. Cooper & T. J. Maguire, 2008. Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89: 439–451.PubMedCrossRefGoogle Scholar
  5. Combes, C., 2001. Parasitism, the Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago.Google Scholar
  6. Deblock, S., 1980. Inventaire des trématodes larvaires parasites des mollusques Hydrobia (Prosobranches) des côtes de France. Parassitologia 22: 1–105.PubMedGoogle Scholar
  7. Doi, H. & N. I. Yurlova, 2011. Host–parasite interactions and global climate oscillations. Parasitology 138: 1022–1028.PubMedCrossRefGoogle Scholar
  8. Elsner, J. & A. Tsonis, 1996. Singular Spectrum Analysis. A New Tool in Time Series Analysis. Plenum Press, New York.CrossRefGoogle Scholar
  9. Ewers, W. H., 1964. The influence of the density of snails on the incidence of larval trematodes. Parasitology 54: 579–583.PubMedCrossRefGoogle Scholar
  10. Fermer, J., S. C. Culloty, T. C. Kelly & R. M. O’Riordan, 2010. Temporal variation of Meiogymnophallus minutus infections in the first and second intermediate host. Journal of Helminthology 84: 362–368.PubMedCrossRefGoogle Scholar
  11. Fredensborg, B. L., K. N. Mouritsen & R. Poulin, 2006. Relating bird host distribution and spatial heterogeneity in trematodes infection in an intertidal snail-from small to large scale. Marine Biology 149: 275–283.CrossRefGoogle Scholar
  12. Galaktionov, K. V., 1983. Microphallids of the “pygmaeus” group. I. Description of species Microphallus pygmaeus (Levinsen, 1881) nec Odhner, 1905 and M. piriformes (Odhner, 1905) nom. nov. (Trematoda: Microphallidae). Vestnik Leningradskogo Universiteta 15(3): 20–30. (in Russian).Google Scholar
  13. Galaktionov, K. V., 1984. Microphallids of the “pygmaeus” group. II. Microphallus triangulatus sp. nov. (Trematoda: Microphallidae). Vestnik Leningradskogo Universiteta 3: 5–11. (in Russian).Google Scholar
  14. Galaktionov, K. V., 1988. Cercariae and metacercariae of Levinseniella brachysoma (Trematoda, Microphallidae) from invertebrates of the White Sea. Parazitologiya 22: 304–311. (in Russian).Google Scholar
  15. Galaktionov, K. V., 1992. Seasonal dynamics of age composition in component populations of daughter sporocyst of microphallids of the “pygmaeus” group (Trematoda, Microphallidae) in the intertidal molluscs Littorina saxatilis in the Barents Sea. Parazitologiya 26: 462–469. (in Russian).Google Scholar
  16. Galaktionov, K. V., 2009. Description of the maritae and determination of the species status of Microphallus pseudopygmaeus sp. nov. (Trematoda: Microphallidae). Parazitologiya 43: 289–299. (in Russian).Google Scholar
  17. Galaktionov, K. V. & A. A. Dobrovolskij, 2003. The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Boston.Google Scholar
  18. Galaktionov, K. V., Irwin, S. W. B., Prokofiev, V. V., Saville, D. H., Nikolaev, K. E. & I. A. Levakin, 2006. Trematode transmission in coastal communities—temperature dependence and climate change perspectives. 11th International Congress of Parasitology (ICOPA XI). Medimond International Proceedings: 85–90.Google Scholar
  19. Golub, G. H. & C. F. van Loan, 1996. Matrix Computations, 3rd edn. The Johns Hopkins University Press, Baltimore.Google Scholar
  20. Golyandina, N., V. Nekrutkin & A. Zhigljavsky, 2001. Analysis of Time Series Structure: SSA and Related Techniques. Chapman & Hall/CRC, Boca Raton.CrossRefGoogle Scholar
  21. Gorbushin, A. M., 1993. Structure of the lines of winter growth interruption and their formation in the shells of Hydrobia ulvae (Gastropoda: Prosobranchia) in the White Sea. Zoologicheskiy Zhurnal 72: 29–34. (in Russian).Google Scholar
  22. Granovitch, A. I., S. O. Sergievsky & I. M. Sokolova, 2000. Spatial and temporal variation of trematode infestation in coexisting populations of intertidal gastropods Littorina saxatilis and L. obtusata in the White Sea. Diseases of Aquatic Organisms 41: 53–64.PubMedCrossRefGoogle Scholar
  23. Hechinger, R. F. & K. D. Lafferty, 2005. Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B 272: 1059–1066.PubMedCrossRefGoogle Scholar
  24. Hudson, P. J., A. P. Dobson & D. Newborn, 2003. Parasitic worms and the population cycles of Red grouse (Lagopus lagopus scoticus). In Berryman, A. (ed.), Population Cycles. Oxford University Press, New York: 109–129.Google Scholar
  25. Hughes, R. N. & P. Answer, 1982. Growth, spawning and trematode infection of Littorina littorea (L.) from an exposed shore in North Wales. Journal of Molluscan Studies 48: 321–330.Google Scholar
  26. Huspeni, T. C. & K. D. Lafferty, 2004. Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Journal of Applied Ecology 14: 795–804.CrossRefGoogle Scholar
  27. Ivanova, T. S., Lajus, D. L., Shatskikh, E. V. & M. V. Ivanov, 2010. Number dynamics of three-spined stickleback in the White Sea: the current state. In Naumov, A. D., A. P. Alekseev & A. A. Sukhotin (eds), Problems of study, rational exploitation and conservation of natural resources of the White Sea. Proceedings of the XI international conference, St. Petersburg, 9–11 November 2010. Zoological Institute of the Russian Academy of Sciences Publishing, St. Petersburg: 59–60 (in Russian).Google Scholar
  28. James, B. L., 1968. The distribution and keys of species in the family Littorinidae and their digenean parasites, in the region of Dale, Pembrokeshire. Field Studies 2: 615–650.Google Scholar
  29. Jolliffe, I. T., 2002. Principal Component Analysis. Series: Springer Series in Statistics, 2nd edn, Vol. XXIX. Springer, New York.Google Scholar
  30. Kennedy, C. R., P. C. Shears & J. A. Shears, 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.PubMedCrossRefGoogle Scholar
  31. Kozminsky, E. V., 2006. Determination of age in Littorina obtusata (Gastropoda, Prosobranchia). Zoologicheskiy Zhurnal 85: 146–157. (in Russian).Google Scholar
  32. Krasnov, Yu. V., 2012. Seabirds of the White Sea: current state of the populations, distribution and trophic connections. In Berger, V. J. (ed.), Biological Resources of the White Sea and their Rational Exploitation. Explorations of Fauna of the Seas, 69(77). Zoological Institute of the Russian Academy of Sciences Publishing, St. Petersburg: 244–260 (in Russian).Google Scholar
  33. Kube, S., J. Kube & A. Bick, 2002a. Component community of larval trematodes in the mudsnail Hydrobia ventrosa: temporal variation in prevalence in relation to host life history. Journal of Parasitology 88: 730–737.PubMedGoogle Scholar
  34. Kube, J., S. Kube & V. Dierschke, 2002b. Spatial and temporal variations in the trematode component community of the mudsnail Hydrobia ventrosa in relation to the occurrence of waterfowl as definitive hosts. Journal of Parasitology 88: 1075–1086.PubMedGoogle Scholar
  35. Lajus, D. L., E. V. Shatskikh, T. S. Ivanova & M. V. Ivanov, 2011. “Waves of life” of three-spined stickleback in the White Sea. In Maximovich, N. V. & I. A. Stogov (eds), Proceedings of XIII scientific workshop “Readings in memory of K. M. Derjugin”. St. Petersburg State University Press, St. Petersburg: 64–98 (in Russian).Google Scholar
  36. Loot, G., M. Aldana & S. A. Navarrete, 2005. Effects of human exclusion on parasitism in intertidal food webs of Central Chile. Conservation Biology 19: 203–212.CrossRefGoogle Scholar
  37. Marcogliese, D. J., 2005. Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35: 705–716.PubMedCrossRefGoogle Scholar
  38. Marcogliese, D. J., T. M. Goater & G. W. Esch, 1990. Crepidostomum cooperi (Allocreadidae) in the burrowing mayfly, Hexagenia limbata (Ephemeroptera) related to trophic status of a lake. American Midland Naturalist 124: 309–317.CrossRefGoogle Scholar
  39. Matthews, P. M., W. I. Montgomery & R. E. B. Hanna, 1985. Infestation of littorinids by larval digenea around a small fishing port. Parasitology 90: 277–287.CrossRefGoogle Scholar
  40. Matveeva, T. A., 1974. The ecology and life cycles of abundant species of the gastropod molluscs of Barents and White Seas. In Khlebovich, V. (ed.), Seasonal Phenomena in the Life of the White and Barents Seas (Explorations of the Fauna of the Seas XIII). Nauka, Leningrad: 65–190.Google Scholar
  41. Merlo, M. J. & J. A. Etchegoin, 2011. Testing temporal stability of the larval digenean community in Heleobia conexa (Mollusca: Cochliopidae) and its possible use as an indicator of environmental fluctuations. Parasitology 138: 249–256.PubMedCrossRefGoogle Scholar
  42. Mouritsen, K. N., 2002. The Hydrobia ulvaeMaritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology 76: 341–347.PubMedCrossRefGoogle Scholar
  43. Mouritsen, K. N. & R. Poulin, 2002. Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124: S101–S117.PubMedGoogle Scholar
  44. Mouritsen, K. N. & R. Poulin, 2010. Parasitism as a determinant of community structure on intertidal flats. Marine Biology 157: 201–213.CrossRefGoogle Scholar
  45. Naumov, A. D., V. J. Berger & K. V. Galaktionov, 2003. Features of White Sea ecosystems: the structure and dynamics of benthic and pelagic communities. Oceanology 43(Suppl 1): S134–S143.Google Scholar
  46. Persson, J., L. C. Stige, N. C. Stenseth, N. Usov, & D. Martynova, 2012. Scale-dependent effects of climate on two copepod species, Calanus glacialis and Pseudocalanus minutus, in an Arctic-boreal sea. Marine Ecology Progress Series (in press).Google Scholar
  47. Poulin, R., 2007. Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ.Google Scholar
  48. Poulin, R. & K. N. Mouritsen, 2003. Large-scale determinants of trematode infections in intertidal gastropods. Marine Ecology Progress Series 254: 187–198.CrossRefGoogle Scholar
  49. Poulin, R. & K. N. Mouritsen, 2006. Climate change, parasitism and the structure of intertidal ecosystems. Journal of Helminthology 80: 183–191.PubMedCrossRefGoogle Scholar
  50. Prokofiev, V. V., 1999. Influence of temperature and salinity on a life span of cercariae of littoral trematodes Cryptocotyle sp. (Heterophyidae), Levinseniella brachysoma and Maritrema subdolum (Microphallidae). Parazitologiya 33: 520–525. (in Russian).Google Scholar
  51. Prokofiev, V. V., 2001. Influence of temperature and salinity on a life span of cercariae of littoral trematodes Podocotyle atomon (Opecoealidae) and Renicola thaidus (Renicolidae). Parazitologiya 35: 69–76. (in Russian).Google Scholar
  52. Reimer, L. W., 1971. Neue Cercarien der Ostsee mit einer Diskussion ihrer möglichen Zuordnung und einem Bestimmungsschlüssel. Parasitologische Schriftenreihe 21: 125–149.Google Scholar
  53. Robson, E. M. & I. C. Williams, 1970. Relationships of some species of Digenea with the marine prosobranch Littorina littorea (L.) I. The occurrence of larval Digenea in L. littorea on the North Yorkshire coast. Journal of Helminthology 44: 153–168.CrossRefGoogle Scholar
  54. Shulman, S. S. & R. E. Shulman-Al’bova, 1953. Parasites of the Fishes of the White Sea. USSR Academy of Sciences Publishing, Moscow. (in Russian).Google Scholar
  55. Skírnisson, K., K. V. Galaktionov & E. V. Kozminsky, 2004. Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland. Journal of Parasitology 90: 50–59.PubMedCrossRefGoogle Scholar
  56. Smith, N. F., 2001. Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologia 127: 115–122.CrossRefGoogle Scholar
  57. Sokal, R. R. & F. J. Rohlf, 1995. Biometry, 3rd edn, 3rd ed. W. H. Freeman, New York.Google Scholar
  58. Stunkard, H. W., 1967. Studies on the Trematode Genus Paramonostomum Lühe, 1909 (Digenea: Notocotylidae). Biological Bulletin 132: 133–145.PubMedCrossRefGoogle Scholar
  59. Thieltges, D. W., 2006. Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559: 455–461.CrossRefGoogle Scholar
  60. Thomas, F., J.-F. Guégan & F. Renaud (eds.), 2009. Ecology and Evolution of Parasitism. Oxford University Press, New York.Google Scholar
  61. Torchin, M. E., K. D. Lafferty & A. M. Kuris, 2002. Parasites and marine invasions. Parasitology 124: S137–S151.CrossRefGoogle Scholar
  62. Usov, N., Martynova, D., Primakov, I. & I. Kutcheva, 2009. Long-term zooplankton dynamics and environment in the White Sea since 1957. From ecosystem function to prediction. In 3rd GLOBEC Open Science Meeting. Victoria, BC, Canada: 126–127.Google Scholar
  63. Valtonen, E. T., E. Helle & R. Poulin, 2004. Stability of Corynosoma populations with fluctuating population densities of the seal definitive host. Parasitology 129: 635–642.PubMedCrossRefGoogle Scholar
  64. Voutilainen, A., T. van Ooik, M. Puurtinen, R. Kortet & J. Taskinen, 2009. Relationship between prevalence of trematode parasite Diplostomum sp. and population density of its snail host Lymnaea stagnalis in lakes and ponds in Finland. Aquatic Ecology 43: 351–357.CrossRefGoogle Scholar
  65. Wilson, R. A. & S. L. Taylor, 1978. The effect of variations in host and parasite density on the level of parasitization of Lymnaea truncatula by Fasciola hepatica. Parasitology 76: 91–98.PubMedCrossRefGoogle Scholar
  66. Yurlova, N. I., S. N. Vodyanitskaya, E. A. Serbina, V. Y. Biserkov, B. B. Georgiev & N. H. Chipev, 2006. Temporal variation in prevalence and abundance of metacercariae in the pulmonate snail Lymnaea stagnalis in Chany Lake, West Siberia, Russia: long-term patterns and environmental covariates. Journal of Parasitology 92: 249–259.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Ivan A. Levakin
    • 1
    • 3
  • Kirill E. Nikolaev
    • 2
    • 3
  • Kirill V. Galaktionov
    • 2
    • 3
  1. 1.The Laboratory of Parasitic Worms, Zoological InstituteRussian Academy of SciencesSt. PetersburgRussia
  2. 2.The White Sea Biological Station, Zoological InstituteRussian Academy of SciencesSt. PetersburgRussia
  3. 3.Department of Invertebrate ZoologySt. Petersburg State UniversitySt. PetersburgRussia

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