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Inventory of organisms interfering with transmission of a marine trematode

  • Jennifer E. Welsh (a1), Jaap van der Meer (a1), Corina P.D. Brussaard (a2) (a3) and David W. Thieltges (a1)

It has increasingly been recognized that organisms can interfere with parasitic free-living stages, preventing them from infecting their specified host and thus reducing infection levels. This common phenomenon in freshwater and terrestrial systems has been termed the ‘dilution effect’ and, so far, is poorly studied in marine systems. Ten common intertidal organisms found in the Dutch Wadden Sea (North Sea) were tested to establish their effects on the free-living cercarial stages of the trematode parasite Himasthla elongata. Most species tested resulted in a significant reduction in cercariae over a 3 hr time period. The amphipod Gammarus marinus removed 100% of the cercariae, while other effective diluters were Crangon crangon (93%), Sargassum muticum (87%), Semibalanus balanoides (71%), Crassostrea gigas (67%), Hemigrapsus takanoi (>54%), Crassostrea gigas shells (44%) and Idotea balthica (24%). In contrast, mixed shells (Cerastoderma edule, Mytilus edulis, Ensis americanus and Littorina littorea) and Fucus versiculosus had no significant effect. These results suggest that dilution effects are widespread in the trematode of H. elongata, with potentially strong effects on its population dynamics.

Corresponding author
Correspondence should be addressed to: J.E. Welsh, Department of Marine Ecology, NIOZ Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, The Netherlands email:
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Bartoli, P. and Boudouresque, C. (1997) Transmission failure of parasites (Digenea) in sites colonized by the recently introduced invasive alga Caulerpa taxifolia. Marine Ecology Progress Series 154, 253260.
Bates, A.E., Leiterer, F., Wiedeback, M.L. and Poulin, R. (2011) Parasitized snails take the heat: a case of host manipulation? Oecologia 167, 613621.
Buschbaum, C., Chapman, A.S. and Saier, B. (2006) How an introduced seaweed can affect epibiota diversity in different coastal systems. Marine Biology 148, 743754.
Desclaux, C., de Montaudouin, X. and Bachelet, G. (2004) Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis. Marine Ecology Progress Series 279, 141150.
Dunne, J.A., Lafferty, K.D., Dobson, A.P., Hechinger, R.F., Kuris, A.M., Martinez, N.D., McLaughlin, J.P., Mouritsen, K.N., Poulin, R., Reise, R., Stouffer, D.B., Thieltges, D.W., Williams, R.J. and Zander, C.D. (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biology 11, e1001579. doi:10.1371/journal.pbio.1001579.
Edelaar, P., Drent, J. and de Goeij, P. (2003) A double test of the parasite manipulation hypothesis in a burrowing bivalve. Oecologia 134, 6671.
Fredensborg, B., Mouritsen, K. and Poulin, R. (2005) Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology Progress Series 290, 109117.
Galaktionov, K.V. and Dobrovolskij, A.A. (2003) The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Dordrecht: Kluwer Academic Publishers.
van der Graaf, S., de Vlas, J., Herlyn, M., Voss, J., Karin, H. and Drent, J. (2009) Macrozoobenthos. Thematic Report No. 10. Wadden Sea Ecosystem No. 25. In Marencic, H. and Vlas, J. de (eds) Quality Status Report 2009. Wadden Sea Ecosystem No. 25. Wilhelmshav: Common Wadden Sea Secretariat, Trilateral Monitoring and Assessment Group.
Harvell, D., Aronson, R., Baron, N., Connell, J., Dobson, A., Ellner, S., Gerber, L., Kim, K., Kuris, A., McCullum, H., Lafferty, K., McKay, B., Porter, J., Pascual, M., Smith, G., Sutherland, K. and Ward, J. (2004) The rising tide of ocean diseases: unsolved problems and research priorities. Frontiers in Ecology and the Environment 2, 375382.
Hopper, J.V., Poulin, R. and Thieltges, D.W. (2008) Buffering role of the intertidal anemone Anthopleura aureoradiata in cercarial transmission from snails to crabs. Journal of Experimental Marine Biology and Ecology 367, 153156.
Jensen, K.T. and Mouritsen, K.N. (1992) Mass mortality in two common soft-bottom invertebrates, Hydrobia ulvae and Corophium volutator-the possible role of trematodes. Helgoländer Meeresuntersuchungen 46, 329339.
Jensen, T., Jensen, K.T. and Mouritsen, K.N. (1998) The influence of the trematode Microphallus claviformis on two congeneric intermediate host species (Corophium): infection characteristics and host survival. Journal of Experimental Marine Biology and Ecology 227, 3548.
Johnson, P.T.J., Dobson, A., Lafferty, K.D., Marcogliese, D.J., Memmott, J., Orlofske, S.A., Poulin, R., and Thieltges, D.W. (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology and Evolution 25, 362371.
Johnson, P.T.J. and Thieltges, D.W. (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961970.
Kaplan, A.T., Rebhal, S., Lafferty, K.D. and Kuris, A.M. (2009) Small estuarine fishes feed on large trematode cercariae: lab and field investigations. Journal of Parasitology 95, 477480.
Keesing, F., Belden, L.K., Daszak, P., Dobson, A., Harvell, C.D., Holt, R.D., Hudso, P., Jolles, A., Jones, K.E., Mitchell, C.E., Myers, S.S., Bogich, T., and Ostfeld, R.S. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647652.
Keesing, F., Holt, R.D. and Ostfeld, R.S. (2006) Effects of species diversity on disease risk. Ecology Letters 9, 485498.
Kelly, D.W., Paterson, R.A., Townsend, C.R., Poulin, R. and Tompkins, D. (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 20472056.
Kopp, K. and Jokela, J. (2007) Resistant invaders can convey benefits to native species. Oikos 116, 295301.
Kuris, A.M., Hechinger, R.F., Shaw, J.C., Whitney, K.L., Aguirre-Macedo, L., Boch, C.A., Dobson, A.P., Dunham, E.J., Fredensborg, B.L., Huspeni, T.C., Lorda, J., Mababal, L., Mancini, F.T., Mora, A.B., Pickering, M., Talhouk, N.L., Torchin, M.E. and Lafferty, K.D. (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515518.
Lafferty, K. (1993) Effects of parasitic castration on growth reproduction and population dynamics of the marine snail Cerithidea californica. Marine Ecology Progress Series 96, 229237.
Lafferty, K.D., Allesina, S., Arim, M., Briggs, C.J., De Leo, G., Dobson, A.P., Dunne, J.A., Johnson, P.T., Kuris, A.M., Marcogliese, D.J., Martinez, N.D., Memmott, J., Marquet, P.A., McLaughlin, J.P., Mordecai, E.A., Pascual, M., Poulin, R. and Thieltges, D.W. (2008) Parasites in food webs: the ultimate missing links. Ecoogy Letters 11, 533546.
Mouritsen, K.N. and Jensen, K.T. (1997) Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series 151, 123134.
Mouritsen, K.N. and Poulin, R. (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101S117.
Mouritsen, K.N. and Poulin, R. (2003) The mud flat anemone–cockle association: mutualism in the intertidal zone? Oecologia 135, 131137.
Pietrock, M. and Marcogliese, D.J. (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.
Prinz, K., Kelly, T.C., O'Riordan, R.M. and Culloty, S.C. (2009) Non-host organisms affect transmission processes in two common trematode parasites of rocky shores. Marine Biology 156, 23032311.
Studer, A., Kremer, L., Nelles, J., Poulin, R. and Thieltges, D.W. (2013) Biotic interference in parasite transmission: can the feeding of anemones counteract an increased risk of parasitism in amphipods at higher temperature? Journal of Experimental Marine Biology and Ecology 445, 116119.
Studer, A. and Poulin, R. (2013) Cercarial survival in an intertidal trematode: a multifactorial experiment with temperature, salinity and ultraviolet radiation. Parasitological Research 112, 243249.
Sweenen, C. (1969) Crawling-tracks of trematode infected Macoma baltica (L.) Netherlands Journal of Sea Research 4, 376379.
Thieltges, D. (2006) Effect of infection by the metacercarial trematodes Renicola roscovita on growth in intertidal blue mussel Mytilus edulis. Marine Ecology Progress Series 319, 129134.
Thieltges, D.W., Bordalo, M.D., Hernández, A.C., Prinz, K. and Jensen, K.T. (2008a) Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135, 11111116.
Thieltges, D.W., Engelsma, M.Y., Wendling, C.C. and Wegner, K.M. (2012) Parasites in the Wadden Sea food web. Journal of Sea Research 82, 122133.
Thieltges, D.W., Jensen, K.T. and Poulin, R. (2008b) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407–26.
Thieltges, D.W., Reise, K., Prinz, K. and Jensen, K.T. (2009) Invaders interfere with native parasite–host interactions. Biological Invasions 11, 14211429.
Thieltges, D.W. and Rick, J. (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae) Diseases of Aquatic Organisms 73, 6368.
Thieltges, D.W., Strasser, M. and Reise, K. (2006) How bad are invaders in coastal waters? The case of the American slipper limpet Crepidula fornicata in western Europe. Biological Invasions 8, 16731680.
Thomas, F., Adamo, S. and Moore, J. (2005) Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185199.
Werding, B. (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Marine Biology 3, 306333.
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