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Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species

Published online by Cambridge University Press:  19 July 2017

JENNIFER E. WELSH ,
CAROLINE LIDDELL ,
JAAP VAN DER MEER  and
DAVID W. THIELTGES
JENNIFER E. WELSH*
Affiliation:
NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, PO Box 59, 1790 AB den Burg, Texel, the Netherlands and Utrecht University, Postbus 80125, 3508 TC, Utrecht, the Netherlands
CAROLINE LIDDELL
Affiliation:
NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, PO Box 59, 1790 AB den Burg, Texel, the Netherlands and Utrecht University, Postbus 80125, 3508 TC, Utrecht, the Netherlands
JAAP VAN DER MEER
Affiliation:
NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, PO Box 59, 1790 AB den Burg, Texel, the Netherlands and Utrecht University, Postbus 80125, 3508 TC, Utrecht, the Netherlands
DAVID W. THIELTGES
Affiliation:
NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, PO Box 59, 1790 AB den Burg, Texel, the Netherlands and Utrecht University, Postbus 80125, 3508 TC, Utrecht, the Netherlands
*
*Corresponding author: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, PO Box 59, 1790 AB den Burg, Texel, the Netherlands. E-mail: [email protected]
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Summary

In parasites with complex life cycles the transmission of free-living infective stages can be influenced by ambient community diversity, in particular via predation. Here, we experimentally investigated whether parasite density and the presence of alternative prey can alter predation rates on free-living cercarial stages of a marine trematode by several non-host predators. All four predator species consumed increasing numbers of cercariae with an increase in cercarial density, indicating that the removal of cercariae by predators is effective over a range of natural densities as well as in the presence of alternative prey for a number of predators typical of marine ecosystems. However, the relative removal rates and the effects of cercarial density and alternative prey differed among predator species. In barnacles and shrimps, significant interactive effects of cercarial density and alternative prey on cercarial predation occurred while in oysters and crabs cercarial removal rates were unaffected by both factors. As changes in cercarial densities directly translate into changes in infection levels in down-stream hosts in this parasite–host system, the observed predator-specific responses suggest that cercarial predation effects on disease risks will depend on the specific species composition of ambient communities and not on non-host biodiversity per se.

Keywords

Transmissiontrematodescercariaepredation
Type
Research Article
Information
Parasitology , Volume 144 , Issue 13 , November 2017 , pp. 1775 - 1782
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Arditi, R. and Ginzburg, L. R. (1989). Coupling in predator-prey dynamics: ratio-dependence. Journal of Theoretical Biology 139, 311–326.Google Scholar
Barillé, L., Prou, J., Héral, M. and Razet, D. (1997). Effects of high natural seston concentrations on the feeding, selection, and absorption of the oyster Crassostrea gigas (Thunberg). Journal of Experimental Marine Biology and Ecology 212, 149–172.Google Scholar
Cognie, B., Barillé, L., Massé, G. and Beninger, P. G. (2003). Selection and processing of large suspended algae in the oyster Crassostrea gigas . Marine Ecology Progress Series 250, 145–152.Google Scholar
Cornell, H. (1976). Search strategies and the adaptive significance of switching in some general predators. American Naturalist 110, 317–320.Google Scholar
Gosling, E. (2003). Bivalve Molluscs: Biology, Ecology and Culture, 1st Edn. John Wiley & Sons, Oxford, UK.Google Scholar
Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A. J., Vandermeer, J. and Wardle, D. A. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.Google Scholar
Jeschke, J. M., Kopp, M. and Tollrian, R. (2004). Consumer-food systems: why Type I functional responses are exclusive to filter feeders. Biological Reviews 79, 337–349.Google Scholar
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, 961–970.Google Scholar
Johnson, P. T., 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, 362–371.Google Scholar
Johnson, P. T., Ostfeld, R. S., & Keesing, F. (2015). Frontiers in research on biodiversity and disease. Ecology letters, 18, 1119–1133.Google Scholar
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485–498.Google Scholar
Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., Hudson, 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, 647–652.Google Scholar
Lafferty, K. D. and Wood, C. L. (2013). It's a myth that protection against disease is a strong and general service of biodiversity conservation: response to Ostfeld and Keesing. Trends in Ecology and Evolution 28, 503–504.Google Scholar
Liddell, C., Welsh, J., van der Meer, J. and Thieltges, D. W. (2017). The effect of dose and frequency of exposure to infectious stages on trematode infection intensity and success in mussels. Diseases of Aquatic Organisms. https://doi.org/10.3354/dao03133.Google Scholar
Magalhães, L., Freitas, R., Dairain, A. and de Montaudouin, X. (2016) Can host density attenuate parasitism? Journal of the Marine Biological Association of the United Kingdom 97, 497–505.Google Scholar
Mouritsen, K. N., McKechnie, S., Meenken, S., Toynbee, J. L. and Poulin, R. (2003) Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density. Journal of the Marine Biological Association of the United Kingdom 83, 307–310.Google Scholar
Murdoch, W. W. (1969). Switching in general predators: experiments on predator specificity and stability of prey populations. Ecological monographs, 39, 335–354.Google Scholar
Oaten, A. and Murdoch, W. W. (1975). Functional response and stability in predator–prey systems. American Naturalist 109, 289–298.Google Scholar
Orlofske, S. A., Jadin, R. C., Preston, D. L. and Johnson, P. T. (2012). Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93, 1247–1253.Google Scholar
Orlofske, S. A., Jadin, R. C. and Johnson, P. T. (2015). It's a predator–eat–parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178, 537–547.Google Scholar
Ostfeld, R. S. and Keesing, F. (2000). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 722–728.Google Scholar
R Core Team (2014). R: A language and environment for statistical computing. R Foundation for statistical Computing, Vienna, Austria. URL http://www.R-project.org/.Google Scholar
RStudio Team (2015). RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. URL http://www.rstudio.com/.Google Scholar
Randolph, S. E. and Dobson, A. D. M. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847–863.Google Scholar
Ren, J. S., Ross, A. H. and Schiel, D. R. (2000). Functional descriptions of feeding and energetics of the Pacific oyster Crassostrea gigas in New Zealand. Marine Ecology Progress Series 208, 119–130.Google Scholar
Ropert, M. and Goulletquer, P. (2000). Comparative physiological energetics of two suspension feeders: polychaete annelid Lanice conchilega (Pallas 1766) and Pacific cupped oyster Crassostrea gigas (Thunberg 1795). Aquaculture 181, 171–189.Google Scholar
Salkeld, D. J., Padgett, K. A. and Jones, J. H. (2013). A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters 16, 679–686.Google Scholar
Schotthoefer, A. M., Labak, K. M. and Beasley, V. R. (2007). Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators. Journal of Parasitology 93, 1240–1243.CrossRefGoogle ScholarPubMed
Schmidt, K. A. and Ostfeld, R. S. (2001). Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619.Google Scholar
Thieltges, D. W. and Reise, K. (2006). Metazoan parasites in intertidal cockles Cerastoderma edule from the northern Wadden Sea. Journal of Sea Research 56, 284–293.Google Scholar
Thieltges, D. W., Krakau, M., Andresen, H., Fottner, S. and Reise, K. (2006). Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgoland Marine Research 60, 307–316.Google Scholar
Thieltges, D. W., Bordalo, M. D., Caballero Hernández, A., Prinz, K. and Jensen, K. T. (2008 a). Ambient fauna impairs parasite transmission in a marine parasite–host system. Parasitology 135, 1111–1116.Google Scholar
Thieltges, D. W., Jensen, K. T. and Poulin, R. (2008 b). The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407–426.Google Scholar
Thieltges, D. W., Reise, K., Prinz, K., & Jensen, K. T. (2009). Invaders interfere with native parasite–host interactions. Biological Invasions, 11, 1421–1429.Google Scholar
van Aken, H. M. (2008). Variability of the water temperature in the western Wadden Sea on tidal to centennial time scales. Journal of Sea Research, 60, 227–234.Google Scholar
van Baalen, M., Křivan, V., van Rijn, P. C. and Sabelis, M. W. (2001). Alternative food, switching predators, and the persistence of predator-prey systems. American Naturalist 157, 512–524.Google Scholar
Welsh, J. E., van der Meer, J., Brussaard, C. P. D. and Thieltges, D. W. (2014) Inventory of organisms interfering with transmission of a marine trematode. Journal of the Marine Biological Association UK 94, 697–702.Google Scholar
Werding, B. (1969). Morphologie, Entwicklung und Okologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Marine Biology 3, 306–333.Google Scholar
Wood, C. L. and Lafferty, K. D. (2013). Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution 28, 239–247.Google Scholar
Worm, B., Barbier, E. B., Beaumont, N., Duffy, J. E., Folke, C., Halpern, B. S., Jackson, J. B. C., Lotze, H. K., Micheli, F., Palumbi, R., Sala, E., Selkoe, K. A., Stachowicz, J. J. and Watson, R. (2006). Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790.Google Scholar
Welsh, J. E., Liddell, C., van der Meer, J. and Thieltges, D. W. (2017). Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species. Royal Netherlands Institute for Sea Research (NIOZ). Dataset http://dx.doi.org/10.4121/uuid:5e8268be-d06e-4ba5-8db3-581172f3565d.Google Scholar
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