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Parasite infectious stages provide essential fatty acids and lipid-rich resources to freshwater consumers

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Abstract

Free-living parasite infectious stages, such as motile cercariae of trematodes (flatworms), can constitute substantial biomass within aquatic ecosystems and are frequently eaten by various consumers, potentially serving as an important source of nutrients and energy. However, quantitative data on their nutritional value (e.g., essential fatty acids [EFA]) are largely lacking. As EFA are leading indicators of nutritional quality and underpin aquatic ecosystem productivity, we performed fatty acid (FA) analysis on an aggregate of ~ 30,000 cercariae of the freshwater trematode, Ribeiroia ondatrae. Individual cercariae contained 15 ng of total FA, and considerable quantities of EFA, including eicosapentaenoic (EPA, at 0.79 ng cercaria−1) and docosahexaenoic (DHA, at 0.01 ng cercaria−1) acids. We estimated annual EFA production by R. ondatrae cercariae for a series of ponds in California to be 40.4–337.0 μg m−2 yr−1 for EPA and 0.7–6.2 μg m−2 yr−1 for DHA. To investigate viability of cercariae as prey, we also compared growth and FA profiles of dragonfly larvae (naiads of Leucorrhinia intacta) fed equivalent masses of either R. ondatrae or zooplankton (Daphnia spp.) for 5 weeks. Naiads raised on the two diets grew equally well, with no significant differences found in their EFA profiles. While zooplankton are widely recognized as a vital source of energy, and an important conduit for the movement of EFA between algae and higher trophic levels, we suggest a similar role for trematode cercariae by ‘unlocking’ EFA from the benthic environment, highlighting their potential importance as a nutrient source that supports animal health.

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References

  • Arts MT, Wainman BC (1999) Lipids in freshwater ecosystems. Springer, New York

    Google Scholar 

  • Arts MT, Brett MT, Kainz MJ (2009) Lipids in aquatic ecosystems. Springer, New York

    Google Scholar 

  • Boissonnot L, Niehoff B, Hagen W, Søreide JE, Graeve M (2016) Lipid turnover reflects life-cycle strategies of small-sized Arctic copepods. J Plankton Res 38:1420–1432

    CAS  Google Scholar 

  • Burdon FJ, Harding JS (2008) The linkage between riparian predators and aquatic insects across a stream-resource spectrum. Freshw Biol 53:330–346

    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

    Google Scholar 

  • Burns CW, Brett MT, Schallenberg M (2011) A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods. Freshw Biol 56:889–903

    Google Scholar 

  • Calder P (2010) Omega-3 fatty acids and inflammatory processes. Nutrients 2:355–374

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Christie WW (1989) The analysis of fatty acids. In: Bala N (ed) Gas chromatography and lipids. PJ Barnes and Associates (The Oily Press), Bridgewater

    Google Scholar 

  • Crews AE, Esch GW (1986) Seasonal dynamics of Halipegus occidualis (Trematoda: Hemiuridae) in Helisoma anceps and its impact on fecundity of the snail host. J Parasitol 72:646–651

    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

    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, Thieltges DW, Williams RJ, Zander CD (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS One 11:e1001579

    CAS  Google Scholar 

  • Fokina N, Ruokolainen T, Bakhmet I (2018) Lipid profiles in Himasthla elongata and their intermediate hosts, Littorina littorea and Mytilus edulis. Mol Biochem Parasitol 225:4–6

    CAS  PubMed  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  • Fried B, Toledo R (2009) The biology of echinostomes. Springer-Verlag, New York

    Google Scholar 

  • Fried B, Rao KS, Sherma J, Huffman JE (1993) Fatty acid composition of Echinostoma trivolvis (Trematoda) rediae and adults and of the digestive gland-gonad complex of Helisoma trivolvis (Gastropoda) infected with the intramolluscan stages of this echinostome. Parasitol Res 79:471–474

    CAS  PubMed  Google Scholar 

  • Fried B, Frazer BA, Kanev I (1998) Comparative observations on cercariae and metacercariae of Echinostoma sp. and Echinoparyphium sp. J Parasitol 84:623–626

    CAS  PubMed  Google Scholar 

  • Fritz KA, Kirschman LJ, McCay SD, Trushenski JT, Warne RW, Whiles MR (2017) Subsidies of essential nutrients from aquatic environments with immune function in terrestrial consumers. Freshw Sci 36:893–900

    Google Scholar 

  • Gladyshev MI, Arts MT, Sushchik NN (2009) Preliminary estimates of the export of omega-3 highly unsaturated fatty acids (EPA + DHA) from aquatic to terrestrial ecosystems. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 179–209

    Google Scholar 

  • Hannon ER, Calhoun DM, Chadalawada S, Johnson PTJ (2017) Circadian rhythms of trematode parasites: applying mixed models to test underlying patterns. Parasitology 145:783–791

    PubMed  Google Scholar 

  • Hoffman D, Boettcher J, Diersen-Schade D (2009) Toward optimizing vision and cognition in term infants by dietary docosahexaenoic and arachidonic acid supplementation: a review of randomized controlled trails. Prostaglandins Leukot Essent Fat Acids 81:151–158

    CAS  Google Scholar 

  • Johnson PT, 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

    PubMed  Google Scholar 

  • Jones DA, Kanazawa A, Ono K (1979) Studies on the nutritional requirements of the larval stages of Penaeus japonicus using microencapsulated diets. Mar Biol 54:261–267

    CAS  Google Scholar 

  • Kabeya N, Fonseca MM, Ferrier DE, Navarro JC, Bay LK, Francis DS, Tocher DR, Castro LFC, Monroig Ó (2018) Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals. Sci Adv 4:aar6849

    Google Scholar 

  • Kainz M, Arts MT, Mazumder A (2004) Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol Oceanogr 49:1784–1793

    CAS  Google Scholar 

  • Kanazawa A, Teshima SI, Sakamoto M (1985) Effects of dietary lipids, fatty acids, and phospholipids on growth and survival of prawn (Penaeus japonicus) larvae. Aquaculture 50:39–49

    CAS  Google Scholar 

  • Kaplan AT, Rebhal S, Lafferty KD, Kuris AM (2009) Small estuarine fishes feed on large trematode cercariae: lab and field investigations. J Parasitol 95:477–480

    PubMed  Google Scholar 

  • Kato C, Iwata T, Wada E (2004) Prey use by web-building spiders: stable isotope analyses of trophic flow at a forest-stream ecotone. Ecol Res 19:633–643

    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

    CAS  PubMed  Google Scholar 

  • Lambden J, Johnson PTJ (2013) Quantifying the biomass of parasites to understand their role in aquatic communities. Ecol Evol 3:2310–2321

    PubMed  PubMed Central  Google Scholar 

  • Lands W (2009) Human life: caught in the food web. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 327–354

    Google Scholar 

  • Lehrter JC, Cebrian J (2010) Uncertainty propagation in an ecosystem nutrient budget. Ecol Appl 20:508–524

    PubMed  Google Scholar 

  • Lombardo P, Cooke GD (2002) Consumption and preference of selected food types by two freshwater gastropod species. Arch Hydrobiol 155:667–685

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Marczak LB, Richardson JS, Claessen MC (2006) Life history phenology and sediment size association of the dragonfly Cordulegaster dorsalis (Odonata: Cordulegastridae) in an ephemeral habitat in southwestern British Columbia. Can Field-Nat 120:347–350

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Marsit CJ, Fried B, Sherma J (2000b) Neutral lipids in cercariae, encysted metacercariae, and rediae of Zygocotyle lunata. J Parasitol 86:1162–1163

    CAS  PubMed  Google Scholar 

  • Martin-Creuzburg D, Kowarik C, Straile D (2017) Cross-ecosystem fluxes: export of polyunsaturated fatty acids from aquatic to terrestrial ecosystems via emerging insects. Sci Total Environ 577:174–182

    CAS  PubMed  Google Scholar 

  • McCauley SJ (2008) Slow, fast and in between: habitat destruction and behavior of larvae in nine species of libellulid dragonfly. Freshwat Biol 53:253–263

    Google Scholar 

  • McDevitt-Galles TM, Johnson PTJJ (2018) Drought attenuates the impact of fish on aquatic macroinvertebrate diversity and species composition. Freshw Biol 63:1457–1468

    CAS  PubMed  PubMed Central  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 14:105–111

    Google Scholar 

  • Moore MN, Halton DW (1975) A histochemical study of the rediae and cercariae of Fasciola hepatica. Parasitol Res 47:45–54

    CAS  Google Scholar 

  • Morley NJ (2011) Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138:1442–1452

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Müller-Navarra DC (1995) Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Arch Hydrobiol 132:297–307

    Google Scholar 

  • Müller-Navarra D, Brett MT, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77

    PubMed  Google Scholar 

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

    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

    PubMed  Google Scholar 

  • Oudejans RCHM, Van der Horst DJ (1974) Effect of excessive fatty acid ingestion upon composition of neutral lipids and phospholipids of snail Helix pomatia. Lipids 9:798–803

    CAS  PubMed  Google Scholar 

  • Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 4–20

    Google Scholar 

  • Paull SH, Johnson PTJ (2018) How temperature, pond-drying, and nutrients influence parasite infection and pathology. EcoHealth 15:396–408

    PubMed  PubMed Central  Google Scholar 

  • Paulson DR (2017) Leucorrhinia intacta. The IUCN red list of threatened species. https://doi.org/10.2305/iucn.uk.20173.rlts.t51274744a65836534.en

  • Peoples RC, Fried B (2008) The effects of various chemical and physical factors on encystment and excystment of Zygocotyle lunata. Parasitol Res 103:899–904

    PubMed  Google Scholar 

  • Pereira ASA, Cavalcanti NL, Nascimento GAF, Nascimento-Silva JLG, Padilha RJR, Viegas LFW, Alves LC, Lima-Filho JL, Chaves MEC (2013) Morphological and morphometric study of cercariae and adult worms of Schistosoma mansoni (SLM strain) isolated from infected mice. Parasitol Res 112:1087–1096

    CAS  PubMed  Google Scholar 

  • Pinowska A (2002) Effects of snail grazing and nutrient release on growth of macrophytes Ceratophyllum demersum and Elodea canadensis and the filamentous green alga Cladophora sp. Hydrobiologia 479:83–94

    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

    PubMed  Google Scholar 

  • Pritchard G (1964) The prey of dragonfly larvae (Odonata; Anisoptera) in ponds in Northern Alberta. Can J Zool 42:785–799

    Google Scholar 

  • Ravet J, Brett MT, Arhonditsis G (2010) The effects of seston lipids on zooplankton fatty acid composition in Lake Washington, Washington, USA. Ecology 91:180–190

    PubMed  Google Scholar 

  • Rosenkranz M, Lagrue C, Poulin R, Selbach C (2018) Small snails, high productivity? Larval output of parasites from an abundant host. Freshwat Biol 63:1602–1609

    Google Scholar 

  • Schariter JA, Pachuski J, Fried B, Sherma J (2002) Determination of neutral lipids and phospholipids in the cercariae of Schistosoma mansoni by high performance thin layer chromatography. J Liq Chromatogr Relat Technol 25:1615–1622

    CAS  Google Scholar 

  • Schindler DE, Scheuerell MD (2002) Habitat coupling in lake ecosystems. Oikos 98:177–189

    Google Scholar 

  • Schmidt KA, Fried B (1997) Prevalence of larval trematodes in Helisoma trivolvis (Gastropoda) from a farm pond in Northampton County, Pennsylvania with special emphasis on Echinostoma trivolvis (Trematoda) cercariae. Proc Helminthol Soc Wash 64:157–159

    Google Scholar 

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

    Google Scholar 

  • Smith TS, Brooks TJ, White HB (1966) Thin-layer and gas-liquid chromatographic analysis of lipid from cercariae of Schistosoma mansoni. Am J Trop Med Hyg 15:307–313

    CAS  PubMed  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

    PubMed  PubMed Central  Google Scholar 

  • Stillwell W, Wassall SR (2003) Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids 126:1–27

    CAS  PubMed  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

    PubMed  Google Scholar 

  • Taipale S, Strandberg U, Peltomaa E, Galloway AWE, Ojala A, Brett M (2013) Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes. Aquat Microb Ecol 71:165–178

    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

    Google Scholar 

  • Thieltges DW, Amundsen PA, Hechinger RF, Johnson PTJ, 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 (2018) Non-host organisms impact transmission at two different life stages in a marine parasite. Parasitol Res 118:111–117

    PubMed  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

    PubMed  Google Scholar 

  • Wissinger SA (1988) Spatial distribution, life history and estimates of survivorship in a fourteen-species assemblage of larval dragonflies (Odonata: Anisoptera). Freshw Biol 20:329–340

    Google Scholar 

  • Wissinger SA (1989) Seasonal variation in the intensity of competition and predation among dragonfly larvae. Ecology 70:1017–1027

    Google Scholar 

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Acknowledgements

The authors thank Travis McDevitt-Galles, Wynne Moss, Lucy Santos and Jamie Nguyen for their assistance, as well as the Blue Oak Ranch and Koffler Scientific Reserves. This work was supported by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (04537-2014 and 05566-2015, respectively) (MTA and JK), as well as the David and Lucile Packard Foundation, the National Science Foundation (1149308, 1754171), and the National Institutes of Health (RI0 GM109499) (PTJJ).

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Authors and Affiliations

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

    Keira M. McKee, Janet Koprivnikar & Michael T. Arts

  2. Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, USA

    Pieter T. J. Johnson

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  1. Keira M. McKee
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  2. Janet Koprivnikar
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  3. Pieter T. J. Johnson
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  4. Michael T. Arts
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KMM, JK and MTA conceived and designed the protocols and laboratory experiments. KMM performed the experiments and fatty acid analysis, as well as statistical analyses in consultation with JK, MTA, and PTJJ. All authors contributed to the manuscript.

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Correspondence to Janet Koprivnikar.

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Communicated by Lisa Belden.

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McKee, K.M., Koprivnikar, J., Johnson, P.T.J. et al. Parasite infectious stages provide essential fatty acids and lipid-rich resources to freshwater consumers. Oecologia 192, 477–488 (2020). https://doi.org/10.1007/s00442-019-04572-0

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