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Patterns of Sphaeridiotrema pseudoglobulus infection in sympatric and allopatric hosts (Bithynia tentaculata) originating from widely separated sites across the USA

  • Immunology and Host-Parasite Interactions - Original Paper
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Abstract

In circumstances where populations of invasive species occur across variable landscapes, interactions among invaders, their parasites, and the surrounding environment may establish local coevolutionary trajectories for the participants. This can generate variable infection patterns when parasites interact with sympatric versus allopatric hosts. Identifying the potential for such patterns within an invasive-species framework is important for better predicting local infection outcomes and their subsequent impacts on the surrounding native community. To begin addressing this question, we exposed an invasive snail (Bithynia tentaculata) from two widely separated sites across the USA (Wisconsin and Montana) to the digenean parasite, Sphaeridiotrema pseudoglobulus, collected from Wisconsin. Parasite exposures generated high infection prevalences in both sympatric and allopatric snails. Furthermore, host survival, host growth, the proportion of patent snails, and the timing of patency did not differ between sympatric and allopatric combinations. Moreover, passaging parasites through snails of different origins had no effect on transmission success to subsequent hosts in the life cycle. However, the number of parasites emerging from snails and the pattern of their release varied based on snail origin. These latter observations suggest the potential for local adaptation in this system, but subsequent research is required to further substantiate this as a key factor underlying infection patterns in the association between S. pseudoglobulus and B. tentaculata.

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References

  • Adlard RD, Miller TL, Snit NJ (2015) The butterfly effect: parasite diversity, environment, and emerging disease in aquatic life. Trends Parasitol 31:160–166

    PubMed  Google Scholar 

  • Alonso A, Castro-Diez P (2008) What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)? Hydrobiologia 614:107–116

    Google Scholar 

  • Bell AS, Sommerville C, Gibson DI (1999) Cercarial emergence of Ichthyocotylurus erraticus (Rudolphi, 1809), I. variegatus (Creplin, 1825) and Apatemon gracilis (Rudolphi, 1819) (Digenea: Strigeidae): contrasting responses to light:dark cycling. Parasitol Res 85:387–392

    CAS  PubMed  Google Scholar 

  • Blackburn TM, Bellard C, Ricciardi A (2019) Alien versus native species as drivers of recent extinctions. Front Ecol Environ 17:203–207

    Google Scholar 

  • Carhart AM, De Jager NR (2019) Spatial and temporal changes in species composition of submersed aquatic vegetation reveal effects of river restoration. Restor Ecol 27:672–682

    Google Scholar 

  • Coelho LHL, Lima WS, Guimaraes MP (2009) Sympatric and allopatric combinations of Lymnaea columella and Fasciola hepatica from southern and south-eastern Brazil. J Helminthol 83:285–288

    CAS  PubMed  Google Scholar 

  • Dar Y, Lounnas M, Djuikwo Teukeng FF, Mouzet R, Courtioux B, Hurtrez-Boussès S, Vignoles P, Dreyfuss G, Rondelaud D (2013) Variations in local adaptation of allopatric Fasciola hepatica to French Galba truncatula in relation to parasite origin. Parasitol Res 112:2543–2549

    CAS  PubMed  Google Scholar 

  • Désy JC, Archambault J-F, Pinel-Alloul B, Hubert J, Campbell PGC (2000) Relationships between total mercury in sediments and methyl mercury in the freshwater gastropod prosobranch Bithynia tentaculata in the St. Lawrence River, Quebec. Can J Fish Aquat Sci 57:164–173

    Google Scholar 

  • Dubois K (2017) American coot mortality and waterbird counts, Georgetown Lake, 2016 Montana Fish, Wildlife & Parks Report 8 p

  • Fleming PB, Huffman DG, Bonner TH, Brandt TM (2011) Metacercarial distribution of Centrocestus formosanus among fish hosts in the Guadalupe River drainage of Texas. J Aquat Anim Health 23:117–124

    PubMed  Google Scholar 

  • Galinier R, Roger E, Mone Y, Duval D, Portet A, Pinaud S et al (2017) A multistrain approach to studying the mechanisms underlying compatibility in the interaction between Biomphalaria glabrata and Schistosoma mansoni. PLoS Negl Trop Dis 11:e0005398

    PubMed  PubMed Central  Google Scholar 

  • Gandon S, Michalakis Y (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. J Evol Biol 15:451–462

    Google Scholar 

  • Gasnier N, Rondelaud D, Abrous M, Carreras F, Boulard C, Diez-Banos P, Cabaret J (2000) Allopatric combination of Fasciola hepatica and Lymnaea truncatula is more efficient than sympatric ones. Int J Parasitol 30:573–578

    CAS  PubMed  Google Scholar 

  • Georgetown Lake Montana (2019) Tempest Technologies. http://georgetownlakemtcom/ Accessed 6 May 2020

  • Gibson GG, Broughton E, Choquette LPE (1972) Waterfowl mortality caused by Cyathocotyle bushiensis Khan, 1962 (Trematoda: Cyathocotylidae), St. Lawrence River, Quebec. Can J Zool 50:1351–1356

    CAS  PubMed  Google Scholar 

  • Hall MD, Ebert D (2012) Disentangling the influence of parasite genotype, host genotype and maternal environment on different stages of bacterial infection in Daphnia magna. Proc R Soc Lond [Biol] 279:3176–3183

    Google Scholar 

  • Hannon ER, Calhoun DM, Chadalawada S, Johnson PTJ (2018) Circadian rhythms of trematode parasites: applying mixed models to test underlying patterns. Parasitology 145:783–791

    PubMed  Google Scholar 

  • Harman WN (2000) Diminishing species richness of mollusks in Oneida Lake, NY, USA. Nautilus 114:120–126

    Google Scholar 

  • Herrmann KK, Sorensen RE (2009) Seasonal dynamics of two mortality-related trematodes using an introduced snail. J Parasitol 95:823–828

    PubMed  Google Scholar 

  • Herrmann KK, Sorensen RE (2011) Differences in natural infections of two mortality-related trematodes in lesser Scaup and American coot. J Parasitol 97:555–558

    PubMed  Google Scholar 

  • Hoeve J, Scott ME (1988) Ecological studies on Cyathocotyle bushiensis (Digenea) and Sphaeridiotrema globulus (Digenea), possible pathogens of dabbling ducks in southern Quebec. J Wildl Dis 24:407–421

    CAS  PubMed  Google Scholar 

  • Horgan FG, Stuart AM, Kudavidanage EP (2014) Impact of invasive apple snails on the functioning and services of natural and managed wetlands Acta Oecologia 54:90–100

  • Ibikounlé M, Mouahid G, Mintsa Nguéma R, Sakiti NG, Kindé-Gasard D, Massougbodji A, Moné H (2012) Life-history traits indicate local adaptation of the schistosome parasite, Schistosoma mansoni, to its snail host, Biomphalaria pfeifferi. Exp Parasitol 132:501–507

    PubMed  Google Scholar 

  • Jokinen E (1992) The freshwater snails (Mollusca: Gastropoda) of New York State. The University of the State of New York, The State Education Department, The New York State Museum, Albany, New York

  • Kaltz O, Shykoff JA (1998) Local adaptation in host–parasite systems. Heredity 81:361–370

    Google Scholar 

  • Karatayev AY, Mastitsky SE, Burlakova LE, Karatayev VA, Hajduk MM, Conn DB (2012) Exotic molluscs in the great lakes host epizootically important trematodes. J Shellfish Res 31:885–894

    Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Google Scholar 

  • Kim DY, Stewart TB, Bauer RW, Mitchell M (2002) Parastrongylus (=Angiostrongylus) cantonensis now endemic in Louisiana wildlife. J Parasitol 88:1024–1026

    CAS  PubMed  Google Scholar 

  • Krist AC, Lively CM, Levri EP, Jokela J (2000) Spatial variation in susceptibility to infection in a snail-trematode interaction. Parasitology 121:395–401

    Google Scholar 

  • Lepitzki DAW, Scott ME, McLaughlin JD (1994) Assessing cercarial transmission of Cyathocotyle bushiensis and Sphaeridiotrema pseudoglobulus by use of sentinel snails. Can J Zool 72:885–891

    Google Scholar 

  • Lima MG, Montresor LC, Pontes J, Augusto RC, Pinheiro da Silva J, Thiengo SC (2019) Compatibility polymorphism based on long-term host-parasite relationships: cross talking between Biomphalaria glabrata and the trematode Schistosoma mansoni from endemic areas in Brazil. Front Immunol 10:328

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lively CM (1989) Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43:1663–1671

    PubMed  Google Scholar 

  • Lively CM (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. Amer Nat 153:S34–S47

    CAS  Google Scholar 

  • Macic V, Albano PG, Almpanidou V, Claudet J, Corrales X, Essl F, Evagelopoulos A, Giovos I, Jimenez C, Kark S, Markovic O, Mazaris AD, Ólafsdóttir GÁ, Panayotova M, Petović S, Rabitsch W, Ramdani M, Rilov G, Tricarico E, Vega Fernández T, Sini M, Trygonis V, Katsanevakis S (2018) Biological invasions in conservation planning: a global systematic review. Front Mar Sci 5:178

    Google Scholar 

  • Manning SD, Woolhouse MEJ, Ndamba J (1995) Geographic compatibility of the freshwater snail Bulinus globosus and schistosomes from the Zimbabwe Highveld. Int J Parasitol 25:37–42

    CAS  PubMed  Google Scholar 

  • McKindsey CW, McLaughlin JD (1994) Hatching dynamics of eggs as further evidence for the existence of two separate species of Sphaeridiotrema (Digenea) in eastern North America. J Helminthol Soc Wash 61:126–127

    Google Scholar 

  • McLaughlin JD, Scott ME, Huffman JE (1993) Sphaeridiotrema globulus (Rud., 1814): evidence for two species known under a single name and a description of Sphaeridiotrema pseudoglobulus n. sp. Can J Zool 71:700–707

    Google Scholar 

  • Menard M, Scott ME (1987) Seasonal occurrence of Cyathocotyle bushiensis Khan, 1962 (Digenea: Cyathocotylidae) metacercariae in the intermediate host Bithynia tentaculata L. (Gastropoda: Prosobranchia). Can J Zool 65:2980–2992

    Google Scholar 

  • Mitchell AJ, Salmon MJ, Huffman DG, Goodwin AE, Brandt TM (2000) Prevalence and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish, the fountain darter, in two Central Texas spring-fed rivers. J Aquat Anim Health 12:283–289

    Google Scholar 

  • Mitchell AJ, Overstreet RM, Goodwin AE, Brandt TM (2005) Spread of an exotic fish-gill trematode: a far reaching and complex problem. Fisheries 30:11–16

    Google Scholar 

  • Morand S, Manning SD, Woolhouse MEJ (1996) Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proc R Soc Lond [Biol] 263:119–128

    CAS  Google Scholar 

  • Munoz-Antoli C, Marin A, Trelis M, Toledo R, Esteban JG (2010) Sympatric and allopatric experimental infections of the planorbid snail, Gyraulus chinensis with miracidia of Euparyphium albuferensis (Trematoda: Echinosotmatidae). J Helminthol 84:420–424

    CAS  PubMed  Google Scholar 

  • Osnas EE, Lively CM (2004) Parasite dose, prevalence of infection and local adaptation in a host-parasite system. Parasitology 128:223–228

    CAS  PubMed  Google Scholar 

  • Perez KE, Werren RL, Lynum CA, Hartman LA, Majoros G, Cole RA (2016) Genetic structure of faucet snail (Bithynia tentaculata) populations in North America based on microsatellite markers. Freshwater Mollusk Biology and Conservation 19:56–68

    Google Scholar 

  • Roy CL, St-Louis V (2017) Spatio-temporal variation in prevalence and intensity of trematodes responsible for waterfowl die-offs in faucet snail-infested waterbodies of Minnesota, USA. Int J Parasitol Parasites and Wildlife 6:162e176

    Google Scholar 

  • Roy CL, St-Louis V, House J (2016) Seasonal distribution of the invasive snail, Bithynia tentaculata, within infested waterbodies in Minnesota, USA, including waterfowl migration. Biol Invasions 18:2923–2941

    Google Scholar 

  • Sandland GJ, Houk S, Walker B, Haro RJ, Gillis R (2013) Differential patterns of infection and life-history expression in native and invasive hosts exposed to a trematode parasite. Hydrobiologia 701:89–98

    Google Scholar 

  • Sandland GJ, Gillis R, Haro RJ, Peirce JP (2014) Infection patterns in invasive and native snail hosts exposed to a parasite associated with waterfowl mortality in the Upper Mississippi River, USA. J Wildl Dis 50:125–129

    PubMed  Google Scholar 

  • Sauer JS, Cole RA, Nissen JM (2007) Finding the exotic faucet snail (Bithynia tentaculata): investigation of waterbird die-offs on the Upper Mississippi River National Wildlife and Fish Refuge. U.S. Geological Survey Open-File Report 2007–1065, 3 p

  • Shostak AW, Esch GW (1990) Photocycle-dependent emergence by cercariae of Halipegus occidualis from Helisoma anceps, with special reference to cercarial emergence patterns as adaptations for transmission. J Parasitol 76:790–795

    Google Scholar 

  • Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, Garcia-Berthou E, Pascal M, Pysek P, Sousa R, Tabacchi E, Vila M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    Google Scholar 

  • Southgate VR, Tchuem Tchuente LA, Theron A, Jourdane J, Ly A, Moncrieff CB, Gryseels B (2000) Compatibility of Schistosoma mansoni Cameroon and Biomphalaria pfeifferi Senegal. Parasitology 121:501–505

    PubMed  Google Scholar 

  • Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55(Suppl. 1):152–174

    Google Scholar 

  • Tchuem Tchuente LA, Southgate VR, Theron A, Jourdane J, Ly A, Gryseels B (1999) Compatibility of Schistosoma mansoni and Biomphalaria pfeifferi in Northern Senegal. Parasitology 118:595–603

    Google Scholar 

  • Teem JL, Qvarnstrom Y, Bishop HS, da Silva AJ, Carter J, White-Mclean J, Smith T (2013) The occurrence of the rat lungworm, Angiostrongylus cantonensis, in nonindigenous snails in the Gulf of Mexico region of the United States. Hawai’i Journal of Medicine & Public Health 72:11–14

    Google Scholar 

  • Theron A (2015) Chronobiology of trematode cercarial emergence: from data recovery to epidemiological, ecological and evolutionary implications. Adv Parasitol 88:123–164

    PubMed  Google Scholar 

  • Theron A, Rognon B, Gourbal B, Mitta G (2014) Multi-parasite host susceptibility and multi-host parasite infectivity: a new approach of the Biomphalaria glabrata/Schistosoma mansoni compatibility polymorphism. Infect Genet Evol 26:80–88

    CAS  PubMed  Google Scholar 

  • Upper Mississippi River Restoration Program Long Term Resource Monitoring (2018) https://umesc.usgs.gov/rivers/upper_mississippi/reach_1/pool_8/pool_8.html Accessed 23 February 2020

  • Weeks AM, De Jager NR, Haro RJ, Sandland GJ (2017) Spatial and temporal relationships between the invasive snail Bithynia tentaculata and submersed aquatic vegetation in Pool 8 of the Upper Mississippi River. River Res Appl 33:729–739

    Google Scholar 

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Acknowledgments

We would like to thank C. Gehri for providing us with the deceased waterfowl and J. Hansen, K. Dubois, and R. Cole for their assistance with selecting collection locations in Montana.

Funding

This work was supported by a grant from the National Science Foundation (NSF-DMS Grant #1852224, “REU Site: Ecological Modeling of the Mississippi River Basin”) awarded to JPP and GJS.

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Authors and Affiliations

  1. Department of Biology, University of Wisconsin-La Crosse, 1725 State Street, La Crosse, WI, 54601, USA

    Gregory J. Sandland

  2. River Studies Center, University of Wisconsin-La Crosse, 1725 State Street, La Crosse, WI, 54601, USA

    Gregory J. Sandland & James P. Peirce

  3. Department of Mathematics, University of Wisconsin-La Crosse, La Crosse, WI, 54601, USA

    James P. Peirce

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  1. Gregory J. Sandland
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  2. James P. Peirce
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GS and JP conceptualized the study, performed the collections, and wrote the manuscript. GS conducted the experiments and analyses.

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Correspondence to Gregory J. Sandland.

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Because our study focused on invertebrate animals, IACUC protocols were not required.

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Section Editor: David Bruce Conn

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Sandland, G.J., Peirce, J.P. Patterns of Sphaeridiotrema pseudoglobulus infection in sympatric and allopatric hosts (Bithynia tentaculata) originating from widely separated sites across the USA. Parasitol Res 120, 187–195 (2021). https://doi.org/10.1007/s00436-020-06949-0

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  • DOI: https://doi.org/10.1007/s00436-020-06949-0

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