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Alternative host identity and lake morphometry drive trematode transmission in brook charr

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Abstract

Both biotic and abiotic factors have been invoked to explain the large variations observed in the prevalence and abundance of parasites in aquatic ecosystems. However, we have only a poor knowledge of the potential interplay among these factors in natural systems. It is, therefore, important to analyze the effects of multiple potential environmental drivers together to get an integrated view of their influence on the prevalence and abundance of parasites. To this end, we selected two genera of digenean trematode parasites that require at least two hosts to complete their life cycle and use two different transmission strategies. Crepidostomum moves through a trophic pathway via consumption of infected prey by the host, while Apophallus infects its hosts via direct penetration of their skin. This study was conducted in 23 Canadian Shield lakes exhibiting orthogonal gradients of biotic (fish species richness and biomass) and abiotic (morphometry, physico-chemical) variables. We quantified prevalence and abundance of these parasites in the skin and intestine of brook charr (Salvelinus fontinalis). Our results show that biotic factors are key drivers of parasite abundance and prevalence, with Apophallus being negatively associated with the fish species richness–biomass gradient, and Crepidostomum responding more to identity of host than to the diversity gradient. Among the abiotic variables, lake area was found to be positively related to both prevalence and abundance in Apophallus. Our results suggest that taking into account the interplay of both biotic and abiotic factors is crucial for understanding patterns of parasite transmission success in boreal lakes.

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References

  • Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conserv Biol 17:267–272

    Article  Google Scholar 

  • Arneberg P, Skorping A, Grenfell B, Read AF (1998) Host densities as determinants of abundance in parasite communities. Proc R Soc B Biol Sci 265:1283–1289

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Stat Softw 67:1–48

    Google Scholar 

  • Bergeron M, Marcogliese DJ, Magnan P (1997) The parasite fauna of brook trout, Salvelinus fontinalis (Mitchill), in relation to lake morphometrics and the introduction of creek chub, Semotilus atromaculatus (Mitchill). Écoscience 4:427–436

    Article  Google Scholar 

  • Bertrand M, Marcogliese DJ, Magnan P (2008) Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. J Fish Biol 72:555–572

    Article  Google Scholar 

  • Bourke P, Magnan P, Rodriguez MA (1999) Phenotypic responses of lacustrine brook charr in relation to the intensity of interspecific competition. Evol Ecol 13:19–31

    Article  Google Scholar 

  • Brownstein JS, Skelly DK, Holford TR, Fish D (2005) Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146:469–475

    Article  PubMed  Google Scholar 

  • Buck JC, Lutterschmidt WI (2017) Parasite abundance decreases with host density: evidence of the encounter-dilution effect for a parasite with a complex life cycle. Hydrobiologia 784:201–210

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York, p 515

    Google Scholar 

  • Calhoun DM, McDevitt-Galles T, Johnson PTJ (2018) Parasites of invasive freshwater fishes and the factors affecting their richness. Freshw Sci 37:134–146

    Article  Google Scholar 

  • Conn DB, Babapulle MN, Klein KA, Rosen DA (1994) Invading the invaders: infestation of zebra mussel by native parasites of the St. Lawrence river. In: Proceedings of the fourth international zebra mussel conference, Madison, Wisconsin pp 515–523

  • Des Clers S (1991) Functional relationship between Sealworm (Pseudoterranova decipiens, Nematoda, Ascaridoidea) burden and host size in Atlantic Cod (Gadus morhua). Proc R Soc B Biol Sci 245:85–89

    Article  CAS  Google Scholar 

  • Desgranges JL, Darveau M (1985) Effect of lake acidity and morphometry on the distribution of aquatic birds in southern Quebec, Canada. Holarct Ecol 8:181–190

    Google Scholar 

  • Dogiel VA, Petrushevskii GK, Polyanski YI (1958) Parasitology of fishes. Leningrad University Press, Saint Petersburg (in Russian; English translation: Olivier & Boyd, London, 1961)

    Google Scholar 

  • Dubois N, Marcogliese DJ, Magnan P (1996) Effects of the introduction of white sucker, Catostomus commersoni, on the parasite fauna of brook trout, Salvelinus fontinalis. Can J Zool 74:1304–1312

    Article  Google Scholar 

  • Dupuch A, Bertolo A, Magnan P, Dill LM (2014) Indirect effects of asymmetrical competition among top predators determine spatial patterns of predation risk for prey. Aquat Sci 76:543–552

    Article  CAS  Google Scholar 

  • Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J (2012) AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249

    Article  Google Scholar 

  • Franz M, Kramer-Schadt S, Greenwood AD, Courtiol A (2018) Sickness-induced lethargy can increase host contact rates and pathogen spread in water-limited landscapes. Funct Ecol 32:2194–2204

    Article  Google Scholar 

  • Giraudoux P, Craig PS, Delattre P, Bao G, Bartholomot B, Harraga S, Quéré JP, Raoul F, Wang Y, Shi D, Vuitton D (2003) Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127:121–131

    Article  Google Scholar 

  • Gorham E (1964) Morphometric control of annual heat budget in temperate lakes. Limnol Oceanogr 9:525–529

    Article  Google Scholar 

  • Grutter AS, Poulin R (1998) Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Mar Ecol Prog Ser 164:263–271

    Article  Google Scholar 

  • Guillemette F, del Giorgio PA (2011) Reconstructing the various facets of dissolved organic carbon bioavailability in freshwater ecosystems. Limnol Oceanogr 56:734–748

    Article  CAS  Google Scholar 

  • Hartvisgen R, Kennedy CR (1993) Patterns in the composition and richness of helminth communities in brown trout, Salmo trutta, in a group of reservoirs. J Fish Biol 43:603–615

    Article  Google Scholar 

  • Hatcher MJ, Dick JT, Dunn AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Front Ecol Environ 10:186–194

    Article  Google Scholar 

  • Hoffman GL (1999) Parasites of North American freshwater fishes, 2nd edn. Cornell University Press, Ithaca

    Google Scholar 

  • Hopkins SR, Ocampo JM, Wojdak JM, Belden LK (2016) Host community composition and defensive symbionts determine trematode parasite abundance in host communities. Ecosphere 7(3):e01278

    Article  Google Scholar 

  • Johnson PTJ, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J Exp Biol 213:961–970

    Article  CAS  PubMed  Google Scholar 

  • Johnson PTJ, Preston DL, Hoverman JT, LaFonte BE (2013) Host and parasite diversity jointly regulate pathogen transmission in complex communities. Proc Natl Acad Sci 110:16916–16921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson PTJ, Wood CL, Joseph MB, Preston DL, Haas SE, Springer YP (2016) Habitat heterogeneity drives the host diversity-begets-parasite diversity relationship: evidence from experimental and field studies. Ecol Lett 19:752–761

    Article  PubMed  PubMed Central  Google Scholar 

  • Keesing F, Holt RD, Ostfeld RS (2006) Effect of species diversity on disease risk. Ecol Lett 9:485–498

    Article  CAS  PubMed  Google Scholar 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Thompkins DM (2009) Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshw Biol 54:1805–1818

    Article  Google Scholar 

  • Kennedy CR, Burrough RJ (1978) Parasites of trout and perch in Malham Tarn. Field Stud J 4:617–629

    Google Scholar 

  • Krakau M, Thieltges DW, Reise K (2006) Native parasites adopt introduced bivalves of the North Sea. Biol Invasion 8:919–925

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  PubMed  Google Scholar 

  • Lachance S, Magnan P (1990a) Performance of domestic, hybrid and wild strains of brook trout, Salvelinus fontinalis, after stocking: the impact of intra- and interspecific competition. Can J Fish Aquat Sci 47:2278–2284

    Article  Google Scholar 

  • Lachance S, Magnan P (1990b) Comparative ecology and reproductive potential of wild, domestic and hybrid strains of brook trout, Salvelinus fontinalis, after stocking. Can J Fish Aquat Sci 47:2285–2292

    Article  Google Scholar 

  • Lafferty KD (2008) Ecosystem consequences of fish parasites. J Fish Biol 73:2083–2093

    Article  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. Ecol Lett 11:533–546

    Article  PubMed  PubMed Central  Google Scholar 

  • Lagrue C, Poulin R (2015) Bottom-up regulation of parasite population densities in freshwater ecosystems. Oikos 124:1639–1647

    Article  Google Scholar 

  • LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci 100:567–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • MacLeod CD, Poulin R (2012) Host-parasite interactions: a litmus test for ocean acidification? Trends Parasitol 28:365–369

    Article  PubMed  Google Scholar 

  • Magnan P (1988) Interactions between brook charr, Salvelinus fontinalis, and nonsalmonid species: ecological shift, morphological shift, and their impact on zooplankton communities. Can J Fish Aquat Sci 45:999–1009

    Article  Google Scholar 

  • Marcogliese DJ, Cone DK (1991) Importance of lake characteristics in structuring parasite communities of salmonids from insular Newfoundland. Can J Zool 69:2962–2967

    Article  Google Scholar 

  • Marcogliese DJ, Cone DK (1997) Parasite communities as indicators of ecosystem stress. Parassitologia 39:227–232

    CAS  PubMed  Google Scholar 

  • Margolis L, Arthur JR (1979) Synopsis of the parasites of fishes of Canada. Bulletin of the Fisheries Research Board of Canada. Bulletin 199

  • Masse D (2000) Le plongeon huard (Gavia immer) sous surveillance en Mauricie. Le Naturaliste canadien 124:22–26

    Google Scholar 

  • Morris DP, Zagarese H, Williamson CE, Balseiro EG, Hargreaves BR, Modenutti B, Moeller R, Queimalinos C (1995) The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol Oceanogr 40:1381–1391

    Article  CAS  Google Scholar 

  • Neilsen LA, Johnson DL (1983) Fisheries techniques. American Fisheries Society, Maryland

    Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PT et al (2016) Vegan: community ecology package. R package version 2.4-1

  • 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

    Article  PubMed  Google Scholar 

  • Österling ME (2011) Test and application of a non-destructive photo-method investigating the parasitic stage of the threatened mussel Margarifitera margarifitera on its host fish Salmo trutta. Biol Conserv 144:2984–2990

    Article  Google Scholar 

  • Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol 20:328–336

    Article  PubMed  Google Scholar 

  • Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266

    Article  Google Scholar 

  • Pietrock M, Marcogliese DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299

    Article  PubMed  Google Scholar 

  • Pitre HN, Boyd FJ (1970) A study of the role of weeds in corn fields in the epidemiology of corn stunt disease. J Econ Entomol 63:195–197

    Article  Google Scholar 

  • Power G (1980) The brook charr, Salvelinus fontinalis. In: Balon EK (ed) Charrs: salmonid fishes of the genus Salvelinus. Dr. W. Junk. Bv Publishers, Hague, pp 141–203

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Sonnenholzner JI, Lafferty KD, Ladah LB (2011) Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galápagos. Ecology 92:2276–2284

    Article  PubMed  Google Scholar 

  • Studer A, Poulin R (2013) Cercarial survival in an intertidal trematode: a multifactorial experiment with temperature, salinity and ultraviolet radiation. Parasitol Res 112:243–249

    Article  CAS  PubMed  Google Scholar 

  • Tremblay S, Magnan P (1991) Interactions between two distantly related species, brook trout (Salvelinus fontinalis) and white sucker (Catostomus commersoni). Can J Fish Aquat Sci 48:857–867

    Article  Google Scholar 

  • Wodjack JM, Edman RM, Wyderko JA, Zemmer SA, Belden LK (2014) Host density and competency determine host diversity effects on infection by trematode parasites. PLoS One 9(8):e105059. https://doi.org/10.1371/journal.pone.0105059

    Article  CAS  Google Scholar 

  • Wyderko JA, Benfield EF, Maerz JC, Cecala KC, Belden LK (2015) Variable infection of stream salamanders in the southern Appalachians by the trematode Metagonimoides oregonensis (family: Heterophyidae). Parasitol Res 114:3159–3165

    Article  PubMed  Google Scholar 

  • Zemmer SA, Wyderko J, Da Silva Neto J, Cedillos I, Clay L, Benfield EF, Belden LK (2017) Seasonal and annual variation in trematode infection of stream snail Eilmia proxima in the southern Appalachian Mountains of Virginia. J Parasitol 103:213–220

    Article  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, p 574

    Book  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgements

We thank Matteo Giacomazzo and David J. Marcogliese for their comments throughout the project. We also thank Laure Devine, Robert Poulin, Lisa Belden (Handling Editor), and two anonymous referees whose constructive comments greatly improved the manuscript. This study was supported by grants from the Canada Research Chair (Grant no. 950-230713) program to PM and the Natural Sciences and Engineering Research Council of Canada (Grant nos. RGPIN-2017-06808 and RGPIN-2017-05451) to PM and AB. A. Filion was supported by a fellowship from the EcoLac NSERC-CREATE Program.

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Authors and Affiliations

  1. Research Centre for Watershed-Aquatic Ecosystem Interactions, Université du Québec à Trois-Rivières, C. P. 500, Trois-Rivières, QC, G9A 5H7, Canada

    Antoine Filion, Vincent Rainville, Marc Pépino, Andrea Bertolo & Pierre Magnan

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  1. Antoine Filion
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  2. Vincent Rainville
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  3. Marc Pépino
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  4. Andrea Bertolo
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  5. Pierre Magnan
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Contributions

PM and AB conceived and designed the study. AF, VR, and MP performed the sampling. AF performed laboratory analyses (parasites) and wrote the first draft of the manuscript. All authors were involved in data analyses, contributed critically to the drafts, and gave final approval for publication.

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Correspondence to Pierre Magnan.

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Communicated by Lisa Belden.

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Filion, A., Rainville, V., Pépino, M. et al. Alternative host identity and lake morphometry drive trematode transmission in brook charr. Oecologia 190, 879–889 (2019). https://doi.org/10.1007/s00442-019-04447-4

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