Direct consumption on free-living cercariae stages of trematodes by non-host organisms interferes with trematode transmission and leads to reduced infections in the next suitable hosts. Consumer functional responses provide a useful tool to examine relationships between consumption rates and ecologically relevant prey densities, whilst also accounting for abiotic factors that likely influence consumption rates. We investigated how temperature influences the consumer functional response of the amphipod Gammarus lacustris towards the cercariae of three freshwater trematodes (Diplostomum, Apatemon and Trichobilharzia). Amphipods displayed different functional responses towards the parasites, with Type II responses for Diplostomum and Type I responses for Apatemon prey. Temperature did not alter the consumption rate of the amphipod predator. Trichobilharzia was likely consumed at similar proportions as Diplostomum; however, this could not be fully evaluated due to low replication. Whilst Type II responses of invertebrate predators are common to various invertebrate prey types, this is the first time a non-filter feeding predator has been shown to exhibit Type I response towards cercarial prey. The prey-specific consumption patterns of amphipods were related to cercarial distribution in the water column rather than to the size of cercariae or temperature influence. The substantial energy flow into food webs by non-host consumer organisms highlights the importance of understanding the mechanisms that modulate functional responses and direct predation in the context of parasitic organisms.

Aquatic Ecology and Centre for Water and Environmental Research University of Duisburg Essen Universitätsstraße 5 D 45141 Essen Germany

Cavanilles Institute for Biodiversity and Evolutionary Biology Science Park University of Valencia P O Box 22085 46071 Valencia Spain

Department of Arctic and Marine Biology Faculty of Biosciences Fisheries and Economics UiT The Arctic University of Norway N9037 Tromsø Norway

Faculty of Science University of South Bohemia in České Budějovice Branišovská 31 37005 České Budějovice Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences 37005 České Budějovice Czech Republic

School of Biosciences Cardiff University Cardiff CF10 3AX UK

The Norwegian Institute for Nature Research P O Box 5685 Torgarden NO 7485 Trondheim Norway

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Bell AS (1996) Studies on the biosystematics and biology of strigeids (Digenea) parasitic in freshwater fish. PhD Dissertation, University of Stirling

Born-Torrijos A, Paterson RA, van Beest GS, Schwelm J, Vyhlídalová T, Henriksen EH, Knudsen R, Kristoffersen R, Amundsen PA, Soldánová M (2020) FR_GammarusPredation, Data from: Temperature does not influence functional response of amphipods consuming different trematode prey. Dryad Digital Repository, 10.5061/dryad.pzgmsbcj4 PubMed PMC

Bovy HC, Barrios-O’Neill D, Emmerson MC, Aldridge DC, Dick JT. Predicting the predatory impacts of the “demon shrimp” Dikerogammarus haemobaphes, on native and previously introduced species. Biol Invasions. 2015;17:597–607. doi: 10.1007/s10530-014-0751-9. DOI

Goedknegt MA, Welsh JE, Drent J, Thieltges DW. Climate change and parasite transmission: how temperature affects parasite infectivity via predation on infective stages. Ecosphere. 2015;6:96. doi: 10.1890/ES15-00016.1. DOI

Haas W, Beran B, Loy C. Selection of the hosts’ habitat by cercariae: from laboratory to the field. J Parasitol. 2008;94:1233–1238. doi: 10.1645/GE-1192.1. PubMed DOI

Hassell MP. A basic model. In: Hassell M, editor. The dynamics of arthropod predator-prey systems. Princeton: Princeton University Press; 1978. pp. 12–27.

Holling CS. Some characteristics of simple types of predation and parasitism. Can Entomol. 1959;91:385–398. doi: 10.4039/Ent91385-7. DOI

Iltis C, Spataro T, Wattier R, Médoc V. Parasitism may alter functional response comparisons: a case study on the killer shrimp Dikerogammarus villosus and two non-invasive gammarids. Biol Invasions. 2018;20:619–632. doi: 10.1007/s10530-017-1563-5. DOI

Jeschke JM, Kopp M, Tollrian R. Consumer food systems: why type I functional responses are exclusive to filter feeders. Biol Rev. 2004;79:337–349. doi: 10.1017/s1464793103006286. PubMed DOI

Johnson PTJ, Dobson A, Lafferty KD, Marcogliese D, Memmott J, Orlofske SA, Poulin R, Thieltges DW. When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol. 2010;25:362–371. doi: 10.1016/j.tree.2010.01.005. PubMed DOI

Juliano SA. Non-linear curve fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J, editors. Design and analysis of ecological experiments. Oxford: Oxford University Press; 2001. pp. 178–196.

Karvonen A, Kirsi S, Hudson PJ, Valtonen ET. Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology. 2004;129:87–92. doi: 10.1017/S0031182004005281. PubMed DOI

Laverty C, Brenner D, McIlwaine C, Lennon JJ, Dick JTA, Lucy FE, Christian KA. Temperature rise and parasitic infection interact to increase the impact of an invasive species. Int J Parasitol. 2017;47:291–296. doi: 10.1016/j.ijpara.2016.12.004. PubMed DOI

Orlofske SA, Jadin RC, Johnson PTJ. It’s a predator-eat-parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia. 2015;178:537–547. doi: 10.1007/s00442-015-3243-4. PubMed DOI

Paterson RA, Dick JTA, Pritchard DW, Ennis M, Hatcher MJ, Dunn AM. Predicting invasive species impacts: a community module functional response approach reveals context dependencies. J Anim Ecol. 2015;84:453–463. doi: 10.1111/1365-2656.12292. PubMed DOI PMC

Poulin R. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology. 2006;132:143–151. doi: 10.1017/S0031182005008693. PubMed DOI

Preston DL, Orlofske SA, Lambden JP, Johnson PTJ. Biomass and productivity of trematode parasites in pond ecosystems. J Anim Ecol. 2013;82:509–517. doi: 10.1111/1365-2656.12030. PubMed DOI

Pritchard DW, Paterson RA, Bovy HC, Barrios-O’Neill D. frair: an R package for fitting and comparing consumer functional responses. Methods Ecol Evol. 2017;8:1528–1534. doi: 10.1111/2041-210X.12784. DOI

R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

Santos MJ, Karvonen A, Pedrot JC, Faltýnková A, Seppälä O, Valtonen ET. Qualitative and quantitative behavioral traits in a community of furcocercariae trematodes: tools for species separation? J Parasitol. 2007;93:1319–1323. doi: 10.1645/GE-1225.1. PubMed DOI

Selbach C, Poulin R. Parasites in space and time: a novel method to assess and illustrate host-searching behaviour of trematode cercariae. Parasitology. 2018;145:1469–1474. doi: 10.1017/S0031182018000288. PubMed DOI

Selbach C, Rosenkranz M, Poulin R. Cercarial behavior determines risk of predation. J Parasitol. 2019;105:330–333. doi: 10.1645/18-165. PubMed DOI

Soldánová M, Selbach C, Sures B. The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLoS One. 2016;11:e0149678. doi: 10.1371/journal.pone.0149678. PubMed DOI PMC

Soldánová M, Georgieva S, Roháčová J, Knudsen R, Kuhn JA, Henriksen EH, Siwertsson A, Shaw JC, Kuris AM, Amundsen P-A, Scholz T, Lafferty KD, Kostadinova A. Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. Int J Parasitol. 2017;47:327–345. doi: 10.1016/j.ijpara.2016.12.008. PubMed DOI

Thieltges DW, Jensen KT, Poulin R. The role biotic factors in the transmission of free-living endohelminth stages. Parasitology. 2008;135:407–426. doi: 10.1017/S0031182007000248. PubMed DOI

Wasserman RJ, Alexander MR, Weyl OLF, Barrios-O’Neill D, Froneman PW, Dalu T. Emergent effects of structural complexity and temperature on predator–prey interactions. Ecosphere. 2016;7:e01239. doi: 10.1002/ecs2.1239. DOI

Welsh JE, Liddell C, van der Meer J, Thieltges DW. Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species. Parasitology. 2017;144:1775–1782. doi: 10.1017/S003182017001056. PubMed DOI

Wilhelm FM, Schindler DW. Effects of Gammarus lacustris (Crustacea: Amphipoda) on plankton community structure in an alpine lake. Can J Fish Aquat Sci. 1999;56:1401–1408. doi: 10.1139/f99-067. DOI

Parasites alter food-web topology of a subarctic lake food web and its pelagic and benthic compartments

Cercariae of a Bird Schistosome Follow a Similar Emergence Pattern under Different Subarctic Conditions: First Experimental Study

Somatic Dimorphism in Cercariae of a Bird Schistosome

Temperature does not influence functional response of amphipods consuming different trematode prey