Skip to main content

Advertisement

SpringerLink
Log in

Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats

  • Review Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Zooplanktonic animals live in the open water of freshwater habitats, whilst trematodes are ubiquitous parasitic worms of aquatic vertebrates and invertebrates. A defining characteristic of trematode life cycles is the cercariae, a mainly planktonic free-living larval stage that emerges into the aquatic environment from infected molluscan hosts. Cercariae are lecithotrophic (non-feeding) larvae analogous of meroplankton. Although millions of planktonic cercariae enter freshwater habitats on a daily basis and are capable of forming into dense clouds, they are a largely neglected component of the zooplankton community, rarely mentioned in faunal studies. Nevertheless, there is increasing evidence to suggest that cercariae have important secondary roles in aquatic food webs and energy transfer. This article reacquaints freshwater biologists with cercariae, highlighting the key characteristics of their biology and population dynamics, their role in food webs, public health and veterinary importance, and the risk of increased population densities under the influence of climate change. The reasons for their neglect in freshwater biology is evaluated and considered to be associated with zooplankton sampling methodologies being unsuitable for collecting cercariae and the paucity of identification keys in the limnological literature.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aoki, Y., K. Sata, N. D. Muhoho, S. I. Noda & E. Kimura, 2003. Cercariometry for detection of transmission sites for schistosomiasis. Parasitology International 52: 403–408.

    Article  PubMed  Google Scholar 

  • Aube, C. I., A. Locke & G. J. Klassen, 2005. Zooplankton communities of a damned estuary in the Bay of Fundy, Canada. Hydrobiologia 548: 127–139.

    Article  Google Scholar 

  • Barnes, R. S. K., P. Calow, P. J. W. Olive, D. W. Golding & J. I. Spicer, 2001. The Invertebrates: a synthesis, 3rd ed. Blackwell Science, Oxford.

    Google Scholar 

  • Bauer, O. N., 1984. Soviet investigations on the population biology of fish parasites. Journal of Fish Biology 25: 545–550.

    Article  Google Scholar 

  • Bauer, O. N., V. L. Vladimirov & N. V. Mindel, 1964. New knowledge about the biology of Strigeata causing mass diseases of fishes. In Ergens, R. & B. Rysavy (eds), Parasitic Worms and Aquatic Conditions. Czechoslovak Academy of Sciences, Prague: 77–82.

    Google Scholar 

  • Bauer, O. N., V. A. Musselius & Y. A. Strelkov, 1973. Diseases of Pond Fishes. Israel Program for Scientific Translations, Jerusalem.

    Google Scholar 

  • Beer, S. A. & S. M. German, 1993. The ecological prerequisites for a worsening of the cercariasis situation in the cities of Russia (exemplified by the Moscow region). Parazitologiia 27: 441–449 [In Russian].

    Google Scholar 

  • Beuret, J. & J. C. Pearson, 1994. Description of a new zygocercous cercaria (Opisthorchioidea: Heterophyidae) from prosobranch gastropods collected at Heron Island (Great Barrier Reef, Australia) and a review of zygocercariae. Systematic Parasitology 27: 105–125.

    Article  Google Scholar 

  • Burks, R. L., D. M. Lodge, E. Jeppesen & T. L. Lauridsen, 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshwater Biology 47: 343–365.

    Article  Google Scholar 

  • Bush, A. O., J. C. Fernandez, G. W. Esch & J. R. Seed, 2001. Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge.

    Google Scholar 

  • Byrne, P., 1995. Seasonal composition of meroplankton in the Dunkellin estuary, Galway Bay. Biology & Environment: Proceedings of the Royal Irish Academy 95B: 35–48.

    Google Scholar 

  • Chernogorenko, M. I., 1982. Periodicity, diurnal rhythm and ecologic factors influencing the rate of issuance of cercariae from mollusc hosts. Hydrobiological Journal 18(3): 64–72.

    Google Scholar 

  • Chubb, J. C., 1979. Seasonal occurence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17: 141–313.

    Article  Google Scholar 

  • Collinge, S. K. & C. Ray, 2006. Disease Ecology Community Structure and Pathogen Dynamics. Oxford University Press, Oxford.

    Google Scholar 

  • Combes, C., 1980. Atlas mondial des cercaires. Memoires du Museum National d’Histoire Naturelle, Serie A, Zoologie 115: 5–235.

    Google Scholar 

  • Combes, C. & A. Theron, 1981. Les densites cercariennes. Memoires du Museum National d’Histoire Naturelle, Serie A, Zoologie 119: 186–196.

    Google Scholar 

  • Combes, C., A. Fournier, H. Mone & A. Theron, 1994. Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109: S3–S13.

    Article  PubMed  Google Scholar 

  • De Gentile, L., H. Picot, P. Bourdeau, R. Bardet, A. Kerjan, M. Piriou, A. Le Guennic, C. Bayssade-Dufour, D. Chabasse & K. E. Mott, 1996. La dermatite cercarienne en Europe: Un problem de santé publique nouveau? Bulletin of the World Health Organization 74: 159–163.

    PubMed  Google Scholar 

  • Dillon, R. T., 2000. The Ecology of Freshwater Molluscs. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Dupuis, A. P. & B. J. Hann, 2009. Climate change, diapause termination and zooplankton population dynamics: an experimental and modelling approach. Freshwater Biology 54: 221–235.

    Article  Google Scholar 

  • Esch, G. W., L. A. Curtis & M. A. Barger, 2001. A perspective on the ecology of trematode communities in snails. Parasitology 123: S57–S75.

    Article  PubMed  Google Scholar 

  • Faltýnková, A., V. Nasincova & L. Kablaskova, 2007a. Larval trematodes (Digenea of the great pond snail, Lymnaea stagnalis (L.) (Gastropoda, Pulmonata) in central Europe: a survey of species and key to their identification. Parasite 14: 39–51.

    PubMed  Google Scholar 

  • Faltýnková, A., K. Niewiadomska, M. J. Santos & E. T. Valtonen, 2007b. Furcocercous cercariae (Trematoda) from freshwater snails in central Finland. Acta Parasitologica 52: 310–317.

    Article  Google Scholar 

  • Faltýnková, A., V. Nasincova & L. Kablaskova, 2008. Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in central Europe: a survey of species and key to their identification. Systematic Parasitology 69: 155–178.

    Article  PubMed  Google Scholar 

  • Fingerut, J. T., C. A. Zimmer & R. K. Zimmer, 2003. Larval swimming overpowers turbulent mixing and facilitates transmission of a marine parasite. Ecology 84: 2502–2515.

    Article  Google Scholar 

  • Frandsen, F. & N. O. Christensen, 1984. An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Tropica 41: 181–202.

    PubMed  CAS  Google Scholar 

  • Galaktionov, K. & A. Dobrovolskij, 2003. The Biology and Evolution of Trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. Kluwer, Dordrecht.

    Google Scholar 

  • Gaschen, H., G. Matthey & P. Jomini, 1956. Un cas de dermatite des nageurs sur les rives du Lac Leman. Bulletin de la Societe de Pathologie Exotique 49: 1172–1177.

    CAS  Google Scholar 

  • George, D. G., 1991. The influence of global warming on freshwater plankton communities in Britain. Freshwater Forum 1: 204–214.

    Google Scholar 

  • Ginetsinskaya, T. A., 1988. Trematodes, Their Life Cycles, Biology and Evolution. Amerind Publishing Company, New Delhi.

    Google Scholar 

  • Grizzle, J. M. & C. J. Brunner, 2009. Infectious diseases of freshwater mussels and other freshwater bivalve molluscs. Reviews in Fisheries Science 17: 425–467.

    Article  Google Scholar 

  • Haas, W., 1994. Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109: S15–S29.

    Article  PubMed  Google Scholar 

  • Haas, W., 2003. Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106: 349–364.

    Article  PubMed  Google Scholar 

  • Haas, W., B. Beran & C. Loy, 2008. Selection of the host’s habitat by cercariae: from laboratory experiments to the field. Journal of Parasitology 94: 1233–1238.

    Article  PubMed  Google Scholar 

  • Harding, J. R., 1978. Cardiff’s tropical disease: cercarial dermatitis. Medical History 22: 83–88.

    PubMed  CAS  Google Scholar 

  • Harvell, C. D., C. E. Mitchell, J. R. Ward, S. Altizer, A. P. Dobson, R. S. Ostfeld & M. D. Samuel, 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296: 2158–2162.

    Article  PubMed  CAS  Google Scholar 

  • Horak, P. & L. Kolarova, 2011. Snails, waterfowl and cercarial dermatitis. Freshwater Biology 56: 779–790.

    Article  Google Scholar 

  • Horne, A. J. & C. R. Goldman, 1994. Limnology, 2nd ed. McGraw-Hill, Inc., New York.

    Google Scholar 

  • Huspeni, T. C., R. F. Hechinger & K. D. Lafferty, 2005. Trematode parasites as estuarine indicators: opportunities, applications, and comparisons with conventional community approaches. In Bortone, S. (ed.), Estuarine Indicators. CRC Press, Boca Raton, FL: 297–314.

    Google Scholar 

  • Hutchinson, G. E., 1967. A Treatise on Limnology II. Introduction to Lake Biology and Limnoplankton. John Wiley & Sons, New York.

    Google Scholar 

  • Jewsbury, J. M., 1985. Effects of water velocity on snails and cercariae. Parasitology Today 1: 116–117.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, P. T. J., A. Dobson, K. D. Lafferty, D. J. Marcogliese, J. Memmott, S. A. Orlofske, R. Poulin & D. W. Thieltges, 2010. When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology & Evolution 25: 362–371.

    Article  Google Scholar 

  • Johnson, M. S., A. Bolick, M. Alexander, D. Huffman, E. Oborny & A. Monroe (2012). Fluctuations in densities of the invasive gill parasite Centrocestus formosanus (Trematoda: Heterophyidae) in the Comal river, Comal county, Texas, USA. Journal of Parasitology (in press).

  • Jordan, P., 1985. Schistosomiasis: The St. Lucia Project. Cambridge University Press, Cambridge.

    Google Scholar 

  • Kaplan, A. T., S. Rebhal, K. D. Lafferty & A. M. Kuris, 2009. Small estuaries fishes feed on large trematode cercariae: lab and field investigations. Journal of Parasitology 95: 477–480.

    Article  PubMed  Google Scholar 

  • Kimura, E., S. Uga, D. K. Migwi, W. R. Mutua, F. M. Kiliku & N. D. Muhoho, 1994. Hourly changes in cercarial densities of Schistosoma haematobium and Schistosoma bovis at different depths in the water and distances from the shore of a dam in Kwale district, Kenya. Tropical Medicine & Parasitology 45: 112–114.

    CAS  Google Scholar 

  • Kozicka, J. & K. Niewiadomska, 1966. A case of the lethal effects of Paralepoderma brumpti (Buttner, 1950) on the fry of Coregonus albula, C. lavaretus and Rutilus rutilus under breeding conditions. Acta Parasitologica Polonica 14: 15–20.

    Google Scholar 

  • Kuris, A. M., R. F. Hechinger, J. C. Shaw, K. L. Whitney, L. Aguirre-Macedo, C. A. Boch, A. P. Dobson, E. J. Dunham, B. L. Fredensborg, T. C. Huspeni, J. Lorda, L. Mababa, F. T. Mancini, A. B. Mora, M. Pickering, N. L. Talhouk, M. E. Torchin & K. D. Lafferty, 2008. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454: 515–518.

    Article  PubMed  CAS  Google Scholar 

  • Lafferty, K. D., A. P. Dobson & A. M. Kuris, 2006. Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103: 11211–11216.

    Article  PubMed  CAS  Google Scholar 

  • Lafferty, K. D., S. Allesina, M. Arim, C. J. Briggs, G. De Leo, A. P. Dobson, J. A. Dunne, P. T. J. Johnson, A. M. Kuris, D. J. Marcogliese, N. D. Martinez, J. Memmott, P. A. Marquet, J. P. McLaughlin, E. A. Mordecai, M. Pascual, R. Poulin & D. W. Thielges, 2008. Parasites in food webs: the ultimate missing links. Ecology Letters 11: 533–546.

    Article  PubMed  Google Scholar 

  • Lapage, G., 1961. A list of the parasitic protozoa, helminths and arthropods recorded from species of the family Anatidae (Ducks, Geese and Swans). Parasitology 51: 1–109.

    Article  CAS  Google Scholar 

  • Lindblade, K. A., 1998. The epidemiology of cercarial dermatitis and its association with limnological characteristics of a northern Michigan lake. Journal of Parasitology 84: 19–23.

    Article  PubMed  CAS  Google Scholar 

  • Lyholt, H. C. K. & K. Buchmann, 1996. Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms 25: 169–173.

    Article  Google Scholar 

  • Macan, T. T., 1959. A Guide to Freshwater Invertebrate Animals. Longman, London.

    Google Scholar 

  • Majoros, G., 1999. Mortality of fish fry as a result of specific and aspecific cercarial invasion under experimental conditions. Acta Veterinaria Hungarica 47: 433–450.

    Article  PubMed  CAS  Google Scholar 

  • Mariani, S., M. J. Uriz & X. Turon, 2003. Methodological bias in the estimations of important meroplanktonic components from near-shore bottoms. Marine Ecology Progress Series 253: 67–75.

    Article  Google Scholar 

  • Mas-Coma, S., M. A. Valero & M. D. Bargues, 2009. Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Veterinary Parasitology 163: 264–280.

    Article  PubMed  Google Scholar 

  • McKenzie, V. J. & A. R. Townsend, 2007. Parasitic and infectious disease responses to changing global nutrient cycles. EcoHealth 4: 384–396.

    Article  Google Scholar 

  • Miracle, M. R., 1974. Niche structure in freshwater zooplankton: a principal components approach. Ecology 55: 1306–1316.

    Article  Google Scholar 

  • Mitchell, A. J., S. Snyder, D. J. Wise & C. C. Mischke, 2007. Evaluating pond shoreline treatments of slurried hydrated lime for reducing marsh rams-horn snail populations. North American Journal of Aquaculture 69: 313–316.

    Article  Google Scholar 

  • Morley, N. J., 2009. Cercarial dermatitis in the UK: a long established history. Clinical and Experimental Dermatology 34: e443.

    Article  PubMed  CAS  Google Scholar 

  • Morley, N. J., 2011. Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138: 1442–1452.

    Article  PubMed  CAS  Google Scholar 

  • Morley, N. J. & J. W. Lewis, 2006. Anthropogenic pressure on a molluscan-trematode community over a long-term period in the Basingstoke canal, UK, and its implications for ecosystem health. Ecohealth 3: 269–280.

    Article  Google Scholar 

  • Morley, N. J., M. E. Adam & J. W. Lewis, 2010. The effects of host size and temperature on the emergence of Echinoparyphium recurvatum cercariae from Lymnaea peregra under natural light conditions. Journal of Helminthology 84: 317–326.

    Article  PubMed  CAS  Google Scholar 

  • Muhoho, N. D., T. Katsumata, E. Kimura, D. K. Migwi, W. R. Mutua, F. M. Kiliku, S. Habe & Y. Aoki, 1997. Cercarial density in the river of an endemic area of Schistosomiasis haematobia in Kenya. American Journal of Tropical Medicine and Hygiene 57: 162–167.

    PubMed  CAS  Google Scholar 

  • Nasir, P., 1984. British Freshwater Cercariae. Universidad de Oriente Press, Cumana, Venezuela.

    Google Scholar 

  • Nasir, P., 1986. North American Freshwater Xiphidiocercariae. Universidad de Oriente Press, Cumana, Venezuela.

    Google Scholar 

  • Okamura, B. & S. W. Feist, 2011. Emerging diseases in freshwater systems. Freshwater Biology 56: 627–637.

    Article  Google Scholar 

  • Pfluger, W., 1980. Experimental epidemiology of Schistosomiasis. I. The prepatent period and cercarial production of Schistosoma mansoni in Biomphalaria snails at various constant temperatures. Zeitschrift fur Parasitenkunde 63: 159–169.

    Article  PubMed  CAS  Google Scholar 

  • Poulin, R., 2006. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132: 143–151.

    Article  PubMed  CAS  Google Scholar 

  • Prentice, M. A. & J. H. Ouma, 1984. Field comparison of mouse immersion and cercariometry for assessing the transmission potential of water containing cercariae of Schistosoma mansoni. Annals of Tropical Medicine and Parasitology 68: 343–352.

    Google Scholar 

  • Rollinson, D. & A. J. G. Simpson, 1987. The Biology of Schistosomes: From Genes to Latrines. Academic Press, London.

    Google Scholar 

  • Smyth, J. D., 1995. Rare, new and emerging helminth zoonoses. Advances in Parasitology 36: 1–45.

    Article  PubMed  CAS  Google Scholar 

  • Stoddart, J. A., 1982. Ingestion of cercariae by a bryozoan. Journal of Parasitology 68: 1137.

    Article  Google Scholar 

  • Susana, J. P., P. Juan, C. Pablo, C. Jorge & G. Bernal, 2008. Water quality and zooplankton composition in a receiving pond of the stormwater runoff from an urban catchment. Journal of Environmental Biology 29: 693–700.

    Google Scholar 

  • Szuroczki, D. & J. M. L. Richardson, 2009. The role of trematode parasites in larval anuran communities: an aquatic ecologist’s guide to the major players. Oecologia 161: 371–385.

    Article  PubMed  Google Scholar 

  • Theron, A., 1986. Cercariometry and the epidemiology of Schistosomiasis. Parasitology Today 2: 61–63.

    Article  PubMed  CAS  Google Scholar 

  • Theron, A., J. P. Pointier & C. Combes, 1978. An ecological study of the involvement of man and rat in the maintenance of transmission of Schistosoma mansoni in Guadeloupe. Annales de Parasitologie Humaine et Comparee 53: 223–234.

    PubMed  CAS  Google Scholar 

  • Thieltges, D. W. & J. Rick, 2006. Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73: 63–68.

    Article  PubMed  Google Scholar 

  • Thieltges, D. W., K. T. Jensen & R. Poulin, 2008a. The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135: 407–426.

    PubMed  CAS  Google Scholar 

  • Thieltges, D. W., X. De Montaudouin, B. Fredensborg, K. T. Jensen, J. Koprivnikar & R. Poulin, 2008b. Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Marine Ecology Progress Series 372: 147–155.

    Article  Google Scholar 

  • Thomas, F., F. Renaud & J.-F. Guegan, 2005. Parasitism and Ecosystems. Oxford University Press, Oxford.

    Book  Google Scholar 

  • Tokobaev, M. M., L. A. Kutikova & N. T. Chibichenko, 1979. The predatory rotifer, Eosphora ehrenbergi, a biological eliminator of cercariae in Lake Issyk-Kul’. Trudy Gel’mintologicheskoi Laboratorii Gel’minty zhivotnykh i rastenii 29: 146–149. [In Russian].

    Google Scholar 

  • Ueda, H. & H. Kimura, 2001. Plankton of spring waters in the Shigenoba River basin. Japanese Journal of Limnology 62: 219–227. [In Japanese].

    Article  CAS  Google Scholar 

  • Upatham, E. S., 1976. Field studies on the bionomics of the free-living stages of St. Lucian Schistosoma mansoni. International Journal for Parasitology 6: 239–245.

    Article  PubMed  CAS  Google Scholar 

  • Voutilainen, A., H. Valdez, A. Karvonen, R. Kortet, H. Kuukka, N. Peuhkuri, J. Piironen & J. Taskinen, 2009. Infectivity of trematode eye flukes in farmed salmonid fish. Effects of parasite and host origins. Aquaculture 293: 108–112.

    Article  Google Scholar 

  • Ward, H. B. & G. C. Whipple, 1918. Freshwater Biology. John Wiley & Sons, New York.

    Google Scholar 

  • Welch, P. S., 1952. Limnology, 2nd ed. McGraw-Hill Book Company, New York.

    Google Scholar 

  • Wesenberg-Lund, C., 1908. Plankton Investigations of the Danish lakes. The Baltic Freshwater Plankton, its Origin and Variation. Gyldendalske Boghandel, Copenhagen, General Part.

    Google Scholar 

  • Wesenberg-Lund, C., 1917. Furesøstudier. Det Kongelige Danske Videnskabers Selskabs Skrifter 8: 1–208.

    Google Scholar 

  • Wesenberg-Lund, C. (1934). Contributions to the development of the Trematoda Digenea. Part II. The Biology of the freshwater cercariae in Danish freshwaters. Memoires de l’Academie Royale des Sciences et des Lettres de Danemark, Copenhague 5(3): 1–223.

  • Wrona, F. J., T. D. Prowse, J. D. Reist, J. E. Hobbie, L. M. J. Levesque & W. F. Vincent, 2006. Climate change effects on aquatic biota, ecosystem structure and function. Ambio 35: 359–369.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguti, S., 1975. A Synoptical Review of Life-Histories of Digenetic Trematodes of Vertebrates. Keigaku Publishing Co, Tokyo.

    Google Scholar 

  • Zbikowska, E., 2011. One snail- three digenea species, different strategies in host-parasite interaction. Animal Biology 61: 1–19.

    Article  Google Scholar 

  • Zimmer, R. K., J. T. Fingerut & C. A. Zimmer, 2009. Dispersal pathways, seed rains, and the dynamics of larval behaviour. Ecology 90: 1933–1947.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

    N. J. Morley

Authors
  1. N. J. Morley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. J. Morley.

Additional information

Handling editor: Karl E. Havens

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morley, N.J. Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 7–19 (2012). https://doi.org/10.1007/s10750-012-1029-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-012-1029-9

Keywords

Search

Navigation