Skip to main content

Advertisement

SpringerLink
Log in

Parasites and their freshwater snail hosts maintain their nutritional value for essential fatty acids despite altered algal diets

  • Ecosystem ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Despite their ubiquity and considerable biomass, the roles played by parasites in aquatic food webs are still not well understood, especially those of their free-living infectious stages. For instance, cercariae, the motile larvae of parasitic flukes (trematodes) may be a key source of nutrients and energy for consumers. As cercariae clonally reproduce within the digestive-gonadal gland complex of gastropod intermediate hosts that acquire nutritionally important polyunsaturated fatty acids (PUFA) mainly from their diets (e.g., by grazing on primary producers), cercariae could transfer snail-derived PUFA if consumed. Through fatty acid (FA) analysis, we explored whether a change in the diet of parasitized hosts altered the FA profiles of both snail-only and trematode-containing snail tissue, thereby affecting their nutritional values. Freshwater snails (Stagnicola elodes) infected with Plagiorchis sp. were fed three different diets (cyanobacteria, green algae, and diatoms) that differed in nutritional quality with respect to FA profiles. While diet influenced the overall FA composition of both snail-only tissue and snail tissue containing trematodes, levels of certain PUFA (mainly omega-3) were largely unaffected. Trematode-containing snail tissue also generally contained more PUFA relative to snail-only tissue. Notably, both tissue types had far higher levels of PUFA than found in their diets. Our results suggest that freshwater snail hosts, and possibly their associated trematode parasites, could be trophic upgraders of key PUFA despite anthropogenically induced changes in algal communities that may lead to overall diminished PUFA contents. As such, cercariae-mediated trophic transfers of PUFA may play important roles in aquatic food webs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acreman J (2013) Culturing microalgae and cyanobacteria: a basic guide. Canadian Phycological Culture Centre (CPCC). University of Waterloo, Waterloo

    Google Scholar 

  • Ahlgren G, Gustafsson I, Boberg M (1992) Fatty acid content and chemical composition of freshwater microalgae. J Phycol 28:37–50

    Article  CAS  Google Scholar 

  • Arakelova KS, Chebotareva MA, Zabelinskii SA (2004) Physiology and lipid metabolism of Littorina saxatilis infected with trematodes. Dis Aquat Org 60:223–231

    Article  CAS  Google Scholar 

  • Babaran D, Arts MT, Botelho RJ, Locke SA, Koprivnikar J (2020) Prospective enzymes for omega-3 PUFA biosynthesis found in endoparasitic classes within the phylum Platyhelminthes. J. Helminthol 94:e212

    Article  CAS  PubMed  Google Scholar 

  • Bec A, Perga M, Koussoroplis A, Bardoux G, Desvilettes C, Bourdier G, Mariotti A (2011) Assessing the reliability of fatty acid–specific stable isotope analysis for trophic studies. Methods Ecol Evol 2:651–659

    Article  Google Scholar 

  • Beers K, Fried B, Fujino T, Sherma J (1995) Effects of diet on the lipid composition of the digestive gland-gonad complex of Biomphalaria glabrata (Gastropoda) infected with larval Echinostoma caproni (Trematoda). Comp Biochem Physiol B Biochemistry Mol Biol 110:729–737

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Brett M, Müller-Navarra D (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshw Biol 38:483–499

    Article  CAS  Google Scholar 

  • Brett MT, Müller-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 

  • Christie WW (1989) The analysis of fatty acids. In: Christie WW (ed) Gas chromatography and lipids. PJ Barnes and Associates (The Oily Press), Bridgewater, UK, pp 36–109

    Google Scholar 

  • Covich AP, Palmer MA, Crowl TA (1999) The role of benthic invertebrate species in freshwater ecosystems: zoobenthic species influence energy flows and nutrient cycling. Bioscience 49:119–127

    Article  Google Scholar 

  • Das UN (2006) Essential fatty acids: biochemistry, physiology and pathology. Biotechnol J 1:420–439

    Article  CAS  PubMed  Google Scholar 

  • De Troch M, Boeckx P, Cnudde C, Van Gansbeke D, Vanreusel A, Vincx M, Caramujo MJ (2012) Bioconversion of fatty acids at the basis of marine food webs: insights from a compound-specific stable isotope analysis. Mar Ecol Prog Ser 465:53–67

    Article  Google Scholar 

  • Dembitsky VM, Kashin AG, Stefanov K (1992) Comparative investigation of phospholipids and fatty acids of freshwater molluscs from the Volga river basin. Comp Biochem Physiol B 102:193–198

    Article  CAS  PubMed  Google Scholar 

  • Dillon RT, Davis KB (1991) The diatoms ingested by freshwater snails: temporal, spatial, and interspecific variation. Hydrobiologia 210:233–242

    Article  Google Scholar 

  • 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 

  • Feiner ZS, Foley CJ, Bootsma HA, Czesny SJ, Janssen J, Rinchard J, Höök TO (2018) Species identity matters when interpreting trophic markers in aquatic food webs. PLoS ONE 13:e0204767

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fried B, Rao KS, Sherma J (1992) Fatty acid composition of Biomphalaria glabrata (Gastropoda: Planorbidae) fed hen’s egg yolk versus leaf lettuce. Comp Biochem Physiol A Physiol 101:351–352

    Article  Google Scholar 

  • Fried B, Rao KS, Sherma J, Huffman JE (1993a) 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

    Article  CAS  PubMed  Google Scholar 

  • Fried B, Rao KS, Sherma J, Huffman JE (1993b) Fatty acid composition of Goniobasis virginica, Physa sp. and Viviparus malleatus (Mollusca: Gastropoda) from Lake Musconetcong, New Jersey. Biochem Syst Ecol 21:809–812

    Article  CAS  Google Scholar 

  • Fried B, Sherma J, Sundar Rao K, Ackman RG (1993c) Fatty acid composition of Biomphalaria glabrata (Gastropoda: Planorbidae) experimentally infected with the intramolluscan stages of Echinostoma caproni (Trematoda). Comp Biochem Physiol B Comp Biochem 104:595–598

    Article  Google Scholar 

  • Fried B, Frazer BA, Lee MS, Sherma J (1998) Thin-layer chromatography and histochemistry analyses of neutral lipids in Helisoma trivolvis infected with four species of larval trematodes. Parasitol Res 84:369–373

    Article  CAS  PubMed  Google Scholar 

  • Furlong ST, Caulfield JP (1988) Schistosoma mansoni: sterol and phospholipid composition of cercariae, schistosomula, and adults. Exp Parasitol 65:222–231

    Article  CAS  PubMed  Google Scholar 

  • Fuschino JR, Guschina IA, Dobson G, Yan ND, Harwood JL, Arts MT (2011) Rising water temperatures alter lipid dynamics and reduce n-3 essential fatty acid concentrations in Scenedesmus obliquus (Chlorophyta). J Phycol 47:763–774

    Article  CAS  PubMed  Google Scholar 

  • Galloway AWE, Winder M (2015) Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS ONE 10:e0130053

    Article  PubMed  PubMed Central  Google Scholar 

  • Galloway AWE, Lowe AT, Sosik EA, Yeung JS, Duggins DO (2013) Fatty acid and stable isotope biomarkers suggest microbe-induced differences in benthic food webs between depths. Limnol Oceanogr 58:1451–1462

    Article  CAS  Google Scholar 

  • Gearhart TA, Ritchie K, Nathan E, Stockwell JD, Kraft J (2017) Alteration of essential fatty acids in secondary consumers across a gradient of cyanobacteria. Hydrobiologia 784:155–170

    Article  CAS  Google Scholar 

  • Gerphagnon M, Agha R, Martin-Creuzburg D, Bec A, Perriere F, Rad-Menéndez C, Gachon CM, Wolinska J (2019) Comparison of sterol and fatty acid profiles of chytrids and their hosts reveals trophic upgrading of nutritionally inadequate phytoplankton by fungal parasites. Environ Microbiol 21:949–958

    Article  CAS  PubMed  Google Scholar 

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

    Chapter  Google Scholar 

  • Glencross BD (2009) Exploring the nutritional demand for essential fatty acids by aquaculture species. Aquaculture 1:71–124

    Article  Google Scholar 

  • Guschina IA, Harwood JL (2009) Algal lipids and effect of the environment on their biochemistry. In: Kainz M, Brett M, Arts M (eds) Lipids in aquatic ecosystems. Springer, New York, pp 1–24

    Google Scholar 

  • Hadley KB, Ryan AS, Forsyth S, Gautier S, Salem N (2016) The essentiality of arachidonic acid in infant development. Nutrients 8:216

    Article  PubMed  PubMed Central  Google Scholar 

  • Hixson SM, Arts MT (2016) Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplankton. Glob Change Biol 22:2744–2755

    Article  Google Scholar 

  • Imhof HK, Laforsch C (2016) Hazardous or not—are adult and juvenile individuals of Potamopyrgus antipodarum affected by non-buoyant microplastic particles? Environ Pollut 218:383–391

    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 

  • Kabeya N, Fonseca MM, Ferrier DEK, Navarro JC, Bay LK, Francis DS, Tocher DR, Castro FC, Monroig Ó (2018) Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals. Sci Adv 4:eaar6849

    Article  PubMed  PubMed Central  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

    Article  CAS  Google Scholar 

  • Kuris A (1990) Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In: Esch GW, Bush AO, Aho JM (eds) Parasite communities: patterns and process. Chapman and Hall, London, pp 69–100

    Chapter  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, Kuris AM (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol 25:564–572

    Article  PubMed  Google Scholar 

  • Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, 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: parasites in food webs. Ecol Lett 11:533–546

    Article  PubMed  PubMed Central  Google Scholar 

  • Lance E, Brient L, Bormans M, Gérard C (2006) Interactions between cyanobacteria and gastropods. Aquat Toxicol 79:140–148

    Article  CAS  PubMed  Google Scholar 

  • Lewert RM, Para BJ (1966) The physiological incorporation of carbon 14 in Schistosoma mansoni cercariae. J Infect Dis 116:171–182

    Article  CAS  PubMed  Google Scholar 

  • Liess A, Hillebrand H (2006) Role of nutrient supply in grazer–periphyton interactions: reciprocal influences of periphyton and grazer nutrient stoichiometry. J N Am Benthol Soc 25:632–642

    Article  Google Scholar 

  • Lundstedt L, Brett MT (1991) Differential growth rates of three cladoceran species in response to mono- and mixed-algal cultures. Limnol Oceanogr 36:159–165

    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 

  • Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sustain Energ Rev 14:217–232

    Article  CAS  Google Scholar 

  • McKee KM, Koprivnikar J, Johnson PTJ, Arts MT (2020) Parasite infectious stages provide essential fatty acids and lipid-rich resources to freshwater consumers. Oecologia 192:477–488

    Article  PubMed  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 

  • Narr CF, Krist AC (2015) Host diet alters trematode replication and elemental composition. Freshw Sci 34:81–91

    Article  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 

  • Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58

    Article  CAS  PubMed  Google Scholar 

  • Parrish CC (2009) Essential fatty acids in aquatic food webs. In: Kainz M, Brett M, Arts M (eds) Lipids in aquatic ecosystems. Springer, New York, pp 309–326

    Chapter  Google Scholar 

  • Parzanini C, Colombo SM, Kainz MJ, Wacker A, Parrish CC, Arts MT (2020) Discrimination between freshwater and marine fish using fatty acids: ecological implications and future perspectives. Environ Rev 28(4):546–559

    Article  Google Scholar 

  • Persson J, Vrede T (2006) Polyunsaturated fatty acids in zooplankton: variation due to taxonomy and trophic position. Freshw Biol 51:887–900

    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 

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

    Article  PubMed  Google Scholar 

  • Rybak AS (2016) Freshwater population of Ulva flexuosa (Ulvaceae, Chlorophyta) as a food source for great pond snail: Lymnaea stagnalis (Mollusca, Lymnaeidae). Phycol Res 64:207–211

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Southgate V (1970) Observations on the effect of the rediae of Fasciola hepatica on the lipid composition of the hepatopancreas of Lymnaea truncatula. Parasitol 61:293–299

    Article  CAS  Google Scholar 

  • Stoknes IS, Økland HM, Falch E, Synnes M (2004) Fatty acid and lipid class composition in eyes and brain from teleosts and elasmobranchs. Comp Biochem Physiol B Biochem Mol Biol 138:183–191

    Article  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

    Article  PubMed  Google Scholar 

  • Taipale SJ, Kainz MJ, Brett MT (2011) Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120:1674–1682

    Article  Google Scholar 

  • Twining CW, Brenna JT, Hairston NG, Flecker AS (2016) Highly unsaturated fatty acids in nature: what we know and what we need to learn. Oikos 125:749–760

    Article  CAS  Google Scholar 

  • Wahlen BD, Willis RM, Seefeldt LC (2011) Biodiesel production by simultaneous extraction and conversion of total lipids from microalgae, cyanobacteria, and wild mixed-cultures. Bioresour Technol 102:2724–2730

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank H. Roshon (CPCC), J. Rohonczy (ECCC), K. Puddephatt, R. Goldberg, T. Smith, A. Williams, and B. Schultz for experimental assistance, as well as L.C. Campbell for advice. This work was supported by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada to MTA and JK (04537-2014 and 05566-2015, respectively). We would also thank the two anonymous reviewers who provided valuable feedback on this manuscript.

Author information

Authors and Affiliations

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

    Dara Babaran, Janet Koprivnikar, Camilla Parzanini & Michael T. Arts

Authors
  1. Dara Babaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Janet Koprivnikar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Camilla Parzanini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael T. Arts
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DB, JK, and MA conceived and designed the experiments. DB performed the experiments. DB and CP analyzed the data, and all authors contributed to writing the manuscript. The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Janet Koprivnikar.

Additional information

Communicated by Jason Todd Hoverman.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 80 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Babaran, D., Koprivnikar, J., Parzanini, C. et al. Parasites and their freshwater snail hosts maintain their nutritional value for essential fatty acids despite altered algal diets. Oecologia 196, 553–564 (2021). https://doi.org/10.1007/s00442-021-04944-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-021-04944-5

Keywords

Search

Navigation