Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-23T22:22:42.394Z Has data issue: false hasContentIssue false
  • English
  • Français

Consumer and host body size effects on the removal of trematode cercariae by ambient communities

Published online by Cambridge University Press:  15 October 2018

Jennifer E. Welsh Open the ORCID record for Jennifer E. Welsh [Opens in a new window] ,
Anke Hempel ,
Mirjana Markovic ,
Jaap van der Meer  and
David W. Thieltges
Jennifer E. Welsh*
Affiliation:
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB den Burg, Texel, the Netherlands
Anke Hempel
Affiliation:
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB den Burg, Texel, the Netherlands
Mirjana Markovic
Affiliation:
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB den Burg, Texel, the Netherlands
Jaap van der Meer
Affiliation:
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB den Burg, Texel, the Netherlands
David W. Thieltges
Affiliation:
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB den Burg, Texel, the Netherlands
*
Author for correspondence: Jennifer E. Welsh, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasite transmission can be altered via the removal of parasites by the ambient communities in which parasite–host interactions take place. However, the mechanisms driving parasite removal remain poorly understood. Using marine trematode cercariae as a model system, we investigated the effects of consumer and host body size on parasite removal rates. Laboratory experiments revealed that consumer or host body size significantly affected cercarial removal rates in crabs, oysters and cockles but not in shrimps. In general, cercarial removal rates increased with consumer (crabs and oysters) and host (cockles) body size. For the filter feeding oysters and cockles, the effects probably relate to their feeding activity which is known to correlate with bivalve size. Low infection levels found in cockle hosts suggest that parasite removal by hosts also leads to significant mortality of infective stages. The size effects of crab and shrimp predators on cercarial removal rates were more complex and did not show an expected size match-mismatch between predators and their cercarial prey, suggesting that parasite removal rates in predators are species-specific. We conclude that to have a comprehensive understanding of parasite removal by ambient communities, more research into the various mechanisms of cercarial removal is required.

Keywords

Parasite–host interactionspredator-prey relationspredator sizetransmission interferencetrematode
Type
Research Article
Information
Parasitology , Volume 146 , Issue 3 , March 2019 , pp. 342 - 347
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beaugrand, G, Brander, KM, Alistair Lindley, J, Souissi, S and Reid, PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426, 661–664.Google Scholar
Brose, U, Jonsson, T, Berlow, E, Warren, P, Banasek-Richter, C, Berier, L-F, Blanchard, JL, Brey, T, Carpenter, SR, Blandenier, CM-F, Cushing, L, Dawah, HA, Dell, T, Edwards, F, Harper-Smith, S, Jacob, U, Ledger, ME, Martinez, ND, Memmott, J, Mintenbeck, K, Pinnegar, JK, Rall, BC, Rayner, TS, Reuman, DC, Ruess, L, Ulrich, W, Williams, RJ, Woodward, G and Cohen, JE (2006) Consumer-resource body-size relationships in natural food webs. Ecology 87, 2411–2417.Google Scholar
Burge, CA, Closek, CJ, Friedman, CS, Groner, ML, Jenkins, CM, Shore-Maggio, A and Welsh, JE (2016) The use of filter-feeders to manage disease in a changing world. Integrative and Comparative Biology 56, 573–587.Google Scholar
Caswell, H (1989) Matrix Population Models: Construction, Analysis, and Interpretation. Sunderland Massachusetts: Sinauer Associates.Google Scholar
Catania, SVL, Koprivnikar, J and Mccauley, SJ (2016) Size-dependent predation alters interactions between parasites and predators. Canadian Journal of Zoology 94, 631–635.Google Scholar
Costa, GC (2009) Predator size, prey size, and dietary niche breadth relationships in marine predators. Ecology 90, 2014–2019.Google Scholar
de Montaudouin, X, Wegeberg, A, Jensen, K and Sauriau, P (1998) Infection characteristics of Himasthla elongata cercariae in cockles as a function of water current. Diseases of Aquatic Organisms 34, 63–70.Google Scholar
de Montaudouin, X, Thieltges, DW, Gam, M, Krakau, M, Pina, S, Bazairi, H, Dabouineau, L, Russell-Pinto, F and Jensen, KT (2009) Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the north-eastern Atlantic shoreline. Journal of the Marine Biological Association of the United Kingdom 89, 543–556.Google Scholar
de Montaudouin, X, Binias, C and Lassalle, G (2012) Assessing parasite community structure in cockles Cerastoderma edule at various spatio-temporal scales. Estuarine, Coastal and Shelf Science 110, 54–60.Google Scholar
Fryxell, JM and Lunberg, P (1998) Individual Behavior and Community Dynamics. London: Chapman & Hall.Google Scholar
Gerlach, SA, Ekstrøm, DK and Eckardt, PB (1976) Filter feeding in the hermit crab, Pagurus bernhardus. Oecologia 24, 257–264.Google Scholar
Gosling, E (2003) Bivalve Molluscs: Biology, Ecology and Culture. Oxford: Blackwell Science.Google Scholar
Jensen, K, Castro, N and Bachelet, G (1999) Infectivity of Himasthla spp. (Trematoda) in cockle (Cerastoderma edule) spat. Journal of the Marine Biological Association of the United Kingdom 79, 265–271.Google Scholar
Johnson, PTJ and Thieltges, DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. The Journal of Experimental Biology 213, 961–970.Google Scholar
Johnson, PTJ, Dobson, A, Lafferty, KD, Marcogliese, DJ, Memmott, J, Orlofske, S, Poulin, R and Thieltges, DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology and Evolution 25, 362–371.Google Scholar
Jones, HD, Richards, OG and Souther, TA (1992) Gill dimensions, water pumping rate and body size in the mussel Mytilus edulis L. Journal of Experimental Marine Biology and Ecology 155, 213–237.Google Scholar
Kaplan, AT, Rebhal, S, Lafferty, KD, Kuris, AM, Biology, M and Science, M (2009) Small estuarine fishes feed on large trematode cercariae: lab and field investigations. Journal of Parasitology 95, 477–480.Google Scholar
Keesing, F, Holt, RD and Ostfeld, RS (2006) Effects of species diversity on disease risk. Ecology Letters 9, 485–498.Google Scholar
Krakau, M, Thieltges, DW and Reise, K (2006) Native parasites adopt introduced bivalves of the North Sea. Biological Invasions 8, 919–925.Google Scholar
Liddell, C, Welsh, JE, Van Der Meer, J and Thieltges, DW (2017) Effect of dose and frequency of exposure to infectious stages on trematode infection intensity and success in mussels. Diseases of Aquatic Organisms 125, 85–92.Google Scholar
Magalhães, L, Freitas, R, Dairain, A and de Montaudouin, X (2017) Can host density attenuate parasitism? Journal of the Marine Biological Association of the United Kingdom 97, 497–505.Google Scholar
Mironova, E, Gopko, M, Pasternak, A, Mikheev, V and Taskinen, J (2018) Trematode cercariae as prey for zooplankton: effect on fitness traits of predators. Parasitology, 1–7. doi: https://doi.org/10.1017/S0031182018000963.Google Scholar
Møhlenberg, F and Riisgård, HU (1979) Filtration rate, using a new indirect technique, in thirteen species of suspension-feeding bivalves. Marine Biology 54, 143–147.Google Scholar
Neill, WE (1975) Experimental studies of microcrustacean competition and resource utilization. Ecology 56, 809–826.Google Scholar
Nilsson, PA and Bronmark, C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88, 539–546.Google Scholar
Orlofske, SA, Jadin, RC, Preston, DL and Johnson, PTJ (2012) Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93, 1247–1253.Google Scholar
Orlofske, SA, Jadin, RC and Johnson, PTJ (2015) It's a predator – eat – parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178, 537–547.Google Scholar
Poulin, R (2011) Evolutionary Ecology of Parasites. Princeton: Princeton University Press.Google Scholar
R Core Development Team (2013) A language and environment for statistical computing.Google Scholar
R Studio Team (2014) RStudio: Integrated Development for R. Version 1.0.143. Boston, MA: RStudio, Inc.Google Scholar
Strasser, M (2002) Reduced epibenthic predation on intertidal bivalves after a severe winter in the European Wadden Sea. Marine Ecology Progress Series 241, 113–123.Google Scholar
Studer, A and Poulin, R (2013) Cercarial survival in an intertidal trematode: a multifactorial experiment with temperature, salinity and ultraviolet radiation. Parasitology Research 112, 243–249.Google Scholar
Thieltges, DW (2008) Effect of host size and temporal exposure on metacercarial infection levels in the intertidal cockle Cerastoderma edule. Journal of the Marine Biological Association of the United Kingdom 88, 613–616.Google Scholar
Thieltges, DW and Reise, K (2007) Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve. Oecologia 150, 569–581.Google Scholar
Thieltges, DW 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, 63–68.Google Scholar
Thieltges, DW, 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, DW, Jensen, KT and Poulin, R (2008 a) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407–426.Google Scholar
Thieltges, DW, Bordalo, MD, Hernández, C, Prinz, K and Jensen, KT (2008 b) Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135, 1111–1116.Google Scholar
Thieltges, DW, Reise, K, Prinz, K and Jensen, KT (2008 c) Invaders interfere with native parasite–host interactions. Biological Invasions 11, 1421–1429.Google Scholar
Watts, AJR, Lewis, C, Goodhead, RM, Beckett, SJ, Moger, J, Tyler, CR and Galloway, TS (2014) Uptake and retention of microplastics by the shore crab Carcinus maenas. Environmental Science & Technology 48, 8823–8830.Google Scholar
Wegeberg, AM, de Montaudouin, X and Jensen, KT (1999) Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatidae, Trematoda). Journal of Experimental Marine Biology and Ecology 238, 259–269.Google Scholar
Welsh, JE, Hempel, A, Markovic, M, van der Meer, J and Thieltges, DW (2018) Consumer and host body size effects on the removal of trematode cercariae by ambient communities. Royal Netherlands Institute for Sea Research (NIOZ). Dataset http://dx.doi.org/10.4121/uuid:63d2d5f0-a4bd-4a08-8f56-a76442423fe4Google Scholar
Welsh, JE, van der Meer, J, Brussaard, CPD and Thieltges, DW (2014) Inventory of organisms interfering with transmission of a marine trematode. Journal of the Marine Biological Association of the United Kingdom 94, 697–702.Google Scholar
Werding, B (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Marine Biology 3, 306–333.Google Scholar