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Free-living parasite infectious stages promote zooplankton abundance under the risk of predation

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Abstract

Free-living parasite infectious stages, such as the cercariae of trematodes (flatworms), can represent substantial biomass in aquatic ecosystems, yet their interactions with other planktonic fauna are poorly understood. Given that cercariae are consumed by various aquatic predators, sometimes even preferentially over zooplankton, their presence may decrease predation pressure on free-living organisms within similar trophic niches by serving as alternate prey. Here, we experimentally examined how the presence of cercariae (Plagiorchis sp.) affected the population dynamics of common freshwater zooplankton (Daphnia sp.) in the presence of a predator (the larval dragonfly, Leucorrhinia intacta) known to consume both. After seeding 48 mesocosms with starting populations of Daphnia, we used four treatments (12 replicates each) representing a factorial combination of the absence/presence of both cercariae and dragonfly larvae and tracked Daphnia populations over 4 weeks. We found a significant interaction between the presence of cercariae and predators on Daphnia population size. When faced with predation pressure, Daphnia reached ~ 50% higher numbers when accompanied by cercariae than without, suggesting a “protective” effect of the latter by acting as substitute prey. Within aquatic ecosystems, an abundance of trematodes may prove advantageous for zooplankton communities that share common predators, but further studies will be needed to determine how this varies depending on the predator, trematode, and zooplankton taxa involved.

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References

  • Akre BG, Johnson DM (1979) Switching and sigmoid functional response curves by damselfly naiads with alternative prey available. J Anim Ecol 48:703–720

    Article  Google Scholar 

  • Andersen T, Hessen DO (1991) Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnol Oceanogr 36(4):807–814

    Article  CAS  Google Scholar 

  • Bernot RJ, Poulin R (2018) Ecological stoichiometry for parasitologists. Trends Parasitol 34:928–933

    Article  PubMed  Google Scholar 

  • Blankespoor H (1970) Host-parasite relationships of an avian trematode, Plagiorchis noblei Park, 1936. PhD Dissertation. Iowa State University Library. http://lib.dr.iastate.edu/cgi/viewcontent.cgi?article=5816&context=rtd. Accessed 5 May 2019

  • Blankespoor HD (1977) Notes on the biology of Plagiorchis noblei Park, 1936 (Trematoda: Plagiorchiidae). Proc Helminthol Soc Wash 44:44–50

    Google Scholar 

  • Brett MT, Goldman CR (1997) Consumer versus resource control in freshwater pelagic food webs. Science 275:384–386

    Article  CAS  PubMed  Google Scholar 

  • Brett MT, Muller-Navarra DC, Ballantyne AP, Ravet JL, Goldman CR (2006) Daphnia fatty acid composition reflects that of their diet. Limnol Oceanogr 51:2428–2437

    Article  CAS  Google Scholar 

  • Burks RL, Jeppesen E, Lodge DM (2001) Pelagic prey and benthic predators: impact of odonate predation on Daphnia. J N Am Benthol Soc 20:615–628

    Article  Google Scholar 

  • Burns CW (1992) Population dynamics of crustacean zooplankton in a mesotrophic lake, with emphasis on Boeckella hamata BREHM (Copepoda: Calanoida). Int Rev Gesamten Hydrobiol 77:553–577

    Article  Google Scholar 

  • Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639

    Article  Google Scholar 

  • Catania SVL, Koprivnikar J, McCauley SJ (2016) Size-dependent predation alters interactions between parasites and predators. Can J Zool 94:631–635

    Article  Google Scholar 

  • Christensen NO (1979) Schistosoma mansoni: interference with cercarial host-finding by various aquatic organisms. J Helminthol 53:7–14

    Article  CAS  PubMed  Google Scholar 

  • Culver DA, Boucherle MM, Bean DJ, Fletcher JW (1985) Biomass of freshwater crustacean zooplankton from length–weight regressions. Can J Fish Aquat Sci 42:1380–1390

    Article  Google Scholar 

  • Dempster SJ, Rau ME (1990) The effects of single exposures of Aedes aegypti larvae and pupae to Plagiorchis noblei cercariae in the laboratory. J Parasitol 76:307–309

    Article  CAS  PubMed  Google Scholar 

  • Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? PNAS 105:11482–11489

    Article  CAS  PubMed  Google Scholar 

  • Dumont HJ, Van de Velde I, Dumont S (1975) The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19:75–97

    Article  PubMed  Google Scholar 

  • Dunne JA, Lafferty KD, Dobson AP, Hechinger RF, Kuris AM, Martinez ND, McLaughlin JP, Mouritsen KN, Poulin R, Reise K, Stouffer DB (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biol 11:e1001579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia. National Center for Biotechnology Information, Bethesda, Md. http://www.ncbi.nlm.nih.gov/books/NBK2042/

  • Esch GW, Barger MA, Fellis KJ (2002) The transmission of digenetic trematodes: style, elegance, complexity. Integr Comp Biol 42:304–312

    Article  PubMed  Google Scholar 

  • Faltýnková A (2005) Larval trematodes (Digenea) in molluscs from small water bodies near Šeské Budšjovice, Czech Republic. Acta Parasitol 50:49–55

    Google Scholar 

  • Fels D, Lee A, Ebert D (2004) The impact of microparasites on the vertical distribution of Daphnia magna. Arch Hydrobiol 161:65–80

    Article  Google Scholar 

  • Ferrari MC, Messier F, Chivers DP (2008) Can prey exhibit threat-sensitive generalization of predator recognition? Extending the predator recognition continuum hypothesis. Proc R Soc Lond B Biol Sci 275:1811–1816

    Article  Google Scholar 

  • Gliwicz ZM, Pijanowska J (1989) The role of predation in zooplankton succession. In: Plankton ecology. Springer, Berlin, pp 253–296

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hansen PJ, Bjørnsen PK (1997) Zooplankton grazing and growth: scaling within the 2–2,000-~µm body size range. Limnol Oceanogr 42:687–704

    Article  Google Scholar 

  • Hanson JM, Peters RH (1984) Empirical prediction of crustacean zooplankton biomass and profundal macrobenthos biomass in lakes. Can J Fish Aquat Sci 41:439–445

    Article  CAS  Google Scholar 

  • Hays GC (2002) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia 503:163–170

    Article  Google Scholar 

  • Hülsmann S, Weiler W (2000) Adult, not juvenile mortality as a major reason for the midsummer decline of a Daphnia population. J Plankton Res 22:151–168

    Article  Google Scholar 

  • Hunt RJ, Swift M (2010) Predation by larval damselflies on cladocerans. J Freshw Ecol 25:345–351

    Article  Google Scholar 

  • Jeffries M (1988) Individual vulnerability to predation: the effect of alternative prey types. Freshwater Biol 19:49–56

    Article  Google Scholar 

  • Johnson PT, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. PNAS 104:15781–15786

    Article  CAS  PubMed  Google Scholar 

  • Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371

    Article  PubMed  Google Scholar 

  • Johnson PTJ, Stanton DE, Forshay KJ, Calhoun DM (2018) Vertically challenged: how disease suppresses Daphnia vertical migration behavior. Limnol Oceanogr 63:886–896

    Article  Google Scholar 

  • Johnston TH, Angel LM (1951) The life history of Plagiorchis jaenschi, a new trematode from the Australian water rat. Trans R Soc S Aust 74:49–58

    Google Scholar 

  • Koprivnikar J, Penalva L (2015) Lesser of two evils? Foraging choices in response to threats of predation and parasitism. PLoS One 10:e0116569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koprivnikar J, Urichuk TMY, Szuroczki D (2017) Influences of habitat and arthropod density on parasitism in two co-occurring host taxa. Can J Zool 95:589–597

    Article  Google Scholar 

  • Koprivnikar J, Riepe TB, Calhoun DM, Johnson PT (2018) Whether larval amphibians school does not affect the parasite aggregation rule: testing the effects of host spatial heterogeneity in field and experimental studies. Oikos 127:99–110

    Article  CAS  Google Scholar 

  • Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson P, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546

    Article  PubMed  PubMed Central  Google Scholar 

  • Lo CT, Lee KM (1996) Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). J Parasitol 82:347–350

    Article  CAS  PubMed  Google Scholar 

  • Loy C, Haas W (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in southern Germany. J Parasitol Res 87:878–882

    Article  CAS  Google Scholar 

  • Lynch M (1979) Predation, competition, and zooplankton community structure: an experimental study. Limnol Oceanog 24:253–272

    Article  Google Scholar 

  • Maloney CL, Field JG (1991) The size-based dynamics of plankton food webs. I. A simulation model of carbon and nitrogen flows. J Plankton Res 13:1003–1038

    Article  Google Scholar 

  • Marcogliese DJ, Cone DK (1997) Food webs: a plea for parasites. Trends Ecol Evol 12:320–325

    Article  CAS  PubMed  Google Scholar 

  • Marsit CJ, Fried B, Sherma J (2000) Neutral lipids in cercariae, encysted metacercariae, and rediae of Echinostoma caproni. J Helminthol 74:365–367

    Article  CAS  PubMed  Google Scholar 

  • McCarthy AM (1999) Photoperiodic cercarial emergence patterns of the digeneans Echinoparyphium recurvatum and Plagiorchis sp. from a mixed infection in Lymnaea peregra. J Helminthol 73:59–62

    Article  Google Scholar 

  • Mironova E, Gopko M, Pasternak A, Mikheev V, Taskinen J (2019) Trematode cercariae as prey for zooplankton: effect on fitness traits of predators. Parasitology 146:105–111

    Article  PubMed  Google Scholar 

  • Morley NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691:7–19

    Article  CAS  Google Scholar 

  • Morley NJ, Lewis JW (2013) Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140:1211–1224

    Article  CAS  Google Scholar 

  • Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:S101–S117

    Article  PubMed  Google Scholar 

  • Orlofske SA, Jadin RC, Preston DL, Johnson PT (2012) Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93:1247–1253

    Article  PubMed  Google Scholar 

  • Orlofske SA, Jadin RC, Johnson PTJ (2015) It’s a predator-eat-parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178:537–547

    Article  PubMed  Google Scholar 

  • Pace ML, Orcutt JD (1981) The relative importance of protozoans, rotifers, and crustaceans in a freshwater zooplankton community. Limnol Oceanogr 26:822–830

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Preston DL, Orlofske SA, Lambden JP, Johnson PTJ (2013) Biomass and productivity of trematode parasites in pond ecosystems. J Anim Ecol 82:509–517

    Article  PubMed  Google Scholar 

  • Rohr JR, Civitello DJ, Crumrine PW, Halstead NT, Miller AD, Schottheofer AM, Stenoien C, Johnson LB, Beasley VR (2015) Predator diversity, intraguild predation, and indirect effects drive parasite transmission. PNAS 112:3008–3013

    Article  CAS  PubMed  Google Scholar 

  • Schell SC (1985) Handbook of trematodes of North America north of Mexico. University of Idaho Press, Moscow

    Google Scholar 

  • Schotthoefer AM, Labak KM, Beasley VR (2007) Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators. J Parasitol 93(5):1240–1243

    Article  PubMed  Google Scholar 

  • Schriver P, Bøgestrond J, Jeppeson E, Søndergaard M (1995) Impact of submerged macrophytes on fish-zooplankton-phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake. Freshw Biol 33:255–270

    Article  Google Scholar 

  • Schwartz SS, Cameron GN (1993) How do parasites cost their hosts? Preliminary answers from trematodes and Daphnia obtusa. Limnol Oceanogr 38:602–612

    Article  Google Scholar 

  • Soldánová M, Selbach C, Sures B (2016) The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLoS One 11:e0149678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szuroczki D, Richardson JM (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 

  • Thieltges DW, de Montaudouin X, Fredensborg B, Jensen KT, Koprivnikar J, Poulin R (2008) Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Mar Ecol Prog Ser 372:147–155

    Article  Google Scholar 

  • Thieltges DW, Amundsen PA, Hechinger RF, Johnson PT, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Zander CD, Poulin R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122:1473–1482

    Google Scholar 

  • Vielma S, Lagrue C, Poulin R, Selbach C (2019) Non-host organisms impact transmission at two different life stages in a marine parasite. Parasitol Res 118:111–117

    Article  PubMed  Google Scholar 

  • Wagenbach GE, Alldredge AL (1974) Effect of light on the emergence pattern of Plagiorchis micracanthos cercariae from Stagnicola exilis. J Parasitol 60:782–785

    Article  CAS  PubMed  Google Scholar 

  • Watertor JL (1965) Intraspecific variation among trematodes of the genus Telorchis. Ph.D. Dissertation. Iowa State University Library. https://doi.org/10.31274/rtd-180813-416

  • Webber RA, Rau ME, Lewis DJ (1986) The effects of various light regimens on the emergence of Plagiorchis noblei cercariae from the molluscan intermediate host, Stagnicola elodes. J Parasitol 72:703–705

    Article  Google Scholar 

  • Weinstein SB, Moura CW, Mendez JF, Lafferty KD (2018) Fear of feces? Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines. Oikos 127:927–934

    Article  Google Scholar 

  • Welsh JE, Liddell C, Van Der Meer J, Thieltges DW (2017) Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species. Parasitology 144:1775–1782

    Article  PubMed  Google Scholar 

  • Wissinger SA (1988) Spatial distribution, life history and estimates of survivorship in a fourteen-species assemblage of larval dragon-flies (Odonata: Anisoptera). Freshw Biol 20:29–340

    Article  Google Scholar 

  • Wojdak JM, Edman RM, Wyderko JA, Zemmer SA, Belden LK (2014) Host density and competency determine the effects of host diversity on trematode parasite infection. PLoS One 9:e105059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, Culver DA (1994) Daphnia population dynamics in western Lake Erie: regulation by food limitation and yellow perch predation. J Great Lakes Res 20:537–545

    Article  Google Scholar 

  • Yoder HR, Coggins JR (1998) Larval trematode assemblages in the snail Lymnaea stagnalis from southeastern Wisconsin. J Parasitol 84:259–268

    Article  CAS  PubMed  Google Scholar 

  • Zakikhani M, Rau ME (1999) Plagiorchis elegans (Digenea: Plagiorchiidae) infections in Stagnicola elodes (Pulmonata: Lymnaeidae): Host susceptibility, growth, reproduction, mortality, and cercarial production. J Parasitol 85:454–463

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank L. Santos and J. Nguyen for experimental assistance, as well as S. J. McCauley for advice. This work was supported by an NSERC Discovery grant to J. K. (RGPIN-2015-05566).

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  1. Department of Chemistry and Biology, Ryerson University, 350 Victoria Street, Toronto, ON, M5B 2K3, Canada

    Ben Schultz & Janet Koprivnikar

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  1. Ben Schultz
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BS and JK conceived and designed the experiments. BS performed the experiments. BS and JK analyzed the data and wrote the manuscript.

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Correspondence to Janet Koprivnikar.

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Additional information

Communicated by Pieter Johnson.

Here we demonstrate that free-living parasite infectious stages interact with other zooplankton and “protect” these by serving as alternative prey, with potentially broad effects of their consumption.

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Schultz, B., Koprivnikar, J. Free-living parasite infectious stages promote zooplankton abundance under the risk of predation. Oecologia 191, 411–420 (2019). https://doi.org/10.1007/s00442-019-04503-z

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