Skip to main content
Log in

Differential infection of exotic and native freshwater amphipods by a parasitic water mold in the St. Lawrence River

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

A parasitic water mold (oomycete) of unknown origin was discovered infecting live native and exotic freshwater gammarid amphipods (Gammarus fasciatus and Echinogammarus ischnus, respectively) in the upper St. Lawrence River. Infections were associated with rapid die-offs of natural populations of amphipods, especially the exotic E. ischnus. Analysis of sequences of three different segments of the rRNA gene cluster indicated that the parasite was in the Saprolegniaceae family, and is related to other crustacean-associated Saprolegniaceae. Specific primers were designed based on the SSU rRNA gene and utilized for semi-quantitative analysis of parasite presence in live and dead amphipods. In laboratory experiments, infection prevalence was higher in E. ischnus individuals than in native amphipods. In addition, dead E. ischnus individuals exhibited more intense infections than G. fasciatus individuals. In contrast to the Great Lakes where E. ischnus has replaced G. fasciatus at many locations, the native species remains abundant in the St. Lawrence River more than a decade after invasion by E. ischnus in the late 1990s. We hypothesize that the parasite is facilitating the co-existence of the two amphipod species by reducing the abundance of E. ischnus in environments in which it might otherwise be dominant.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Barron GL (2004) Fungal parasites and predators of rotifers, nematodes, and other invertebrates. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi. Elsevier, Amsterdam, pp 435–450

    Chapter  Google Scholar 

  • Bly JE, Lawson LA, Szalai AJ, Clem LW (1993) Environmental factors affecting outbreaks of winter saprolegniosis in channel catfish, Ictalurus punctatus (Rafinesque). J Fish Dis 16:541–549

    Article  Google Scholar 

  • Boisclair D, Leggett WC (1989) Among-population variability of fish growth: II. Influence of prey type. Can J Fish Aquat Sci 46:468–482

    Article  Google Scholar 

  • Cerenius L, Söderhäll K, Persson M, Ajaxon R (1988) The crayfish plague fungus, Aphanomyces astaci—diagnosis, isolation, and pathobiology. Freshw Crayfish 7:131–144

    Google Scholar 

  • deRivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376

    Article  Google Scholar 

  • Dermott R, Witt J, Um EM, Gonzalez M (1998) Distribution of the Ponto-Caspian amphipod Echinogammarus ischnus in the Great Lakes and replacement of native Gammarus fasciatus. J Great Lakes Res 24:442–452

    Article  Google Scholar 

  • Dick MW, Vick MC, Gibbings JG, Hedderson TA, Lastra CCL (1999) 18S rDNA for species of Leptolegnia and other Peronosporomycetes: justification for the subclass taxa Saprolegniomycetidae and Peronosporomycetidae and division of the Saprolegniaceae sensu lato into the Leptolegniaceae and Saprolegniaceae. Mycol Res 103:1119–1125

    Article  CAS  Google Scholar 

  • Diéguez-Uribeondo J, Söderhäll K (1993) Procambarus clarkii Girard as a vector for the crayfish plague fungus, Aphanomyces ascaci Schikora. Aquac Fish Manag 24:761–765

    Google Scholar 

  • Dunn AM, Dick JTA (1998) Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland. Ecography 21:593–598

    Article  Google Scholar 

  • Dunn JC, McClymont HE, Christmas M, Dunn AM (2009) Competition and parasitism in the native White Clawed Crayfish Austropotamobius pallipes and the invasive Signal Crayfish Pacifastacus leniusculus in the UK. Biol Invasions 11:315–324

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gouda HA, Moharram AM (2009) A novel Salifa-Saprolegnia association. J Invertebr Pathol 101:23–28

    Article  PubMed  Google Scholar 

  • Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520

    Article  Google Scholar 

  • Hunt CE, Yamada SB (2003) Biotic resistance experienced by an invasive crustacean in a temperate estuary. Biol Invasions 5:33–43

    Article  Google Scholar 

  • Johnson PT (1985) Parasites of benthic amphipods: microsporidians of Ampelisca agassizi (Judd) and some other gammarideans. Fish Bull 83:497–505

    Google Scholar 

  • Johnson PT (1986a) Parasites of benthic amphipods—ciliates. Fish Bull 84:204–209

    Google Scholar 

  • Johnson PT (1986b) Parasites of benthic amphipods: dinoflagellates (Duboscquodinida: Syndinidae). Fish Bull 84:605–614

    Google Scholar 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

    Article  CAS  PubMed  Google Scholar 

  • Kestrup ÅM, Ricciardi A (2009) Environmental heterogeneity limits the local dominance of an invasive freshwater crustacean. Biol Invasions 11:2095–2105

    Article  Google Scholar 

  • Kiziewicz B, Nalepa TF (2008) Some fungi and water molds in waters of Lake Michigan with emphasis on those associated with the benthic amphipod Diporeia spp. J Great Lakes Res 34:774–780

    Google Scholar 

  • Kozubikova E, Petrusek A, Duris Z, Martin MP, Dieguez-Uribeondo J, Oidtmann B (2008) The old menace is back: recent crayfish plague outbreaks in the Czech Republic. Aquaculture 274:208–217

    Article  Google Scholar 

  • Leano EM, Vrijmoed LLP, Jones EBG (1999) Saprolegnia diclina isolated from pond cultured red drum (Sciaenops ocellatus) in Hong Kong. Mycol Res 103:701–706

    Article  Google Scholar 

  • Lopez-Garcia P, Rodriguez-Valera F, Pedros-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607

    Article  CAS  PubMed  Google Scholar 

  • MacNeil C, Dick JTA, Elwood RW (1997) The trophic ecology of freshwater Gammarus spp. (Crustacea: Amphipoda): problems and perspectives concerning the functional feeding group concept. Biol Rev 72:349–364

    Article  Google Scholar 

  • MacNeil C, Dick JTA, Hatcher MJ, Terry RS, Smith JE, Dunn AM (2003a) Parasite-mediated predation between native and invasive amphipods. Proc R Soc Lond B Biol Sci 270:1309–1314

    Article  Google Scholar 

  • MacNeil C, Fielding NJ, Dick JTA, Briffa M, Prenter J, Hatcher MJ, Dunn AM (2003b) An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea). Freshw Biol 48:2085–2093

    Article  Google Scholar 

  • Moon-van der Staay SY, van der Staay GWM, Guillou L, Vaulot D, Claustre H, Medlin LK (2000) Abundance and diversity of prymnesiophytes in the picoplankton community from the equatorial Pacific Ocean inferred from 18S rDNA sequences. Limnol Oceanogr 45:98–109

    Article  CAS  Google Scholar 

  • Nechwatal J, Mendgen K (2006) Pythium litorale sp nov., a new species from the littoral of Lake Constance, Germany. FEMS Microbiol Lett 255:96–101

    Article  CAS  PubMed  Google Scholar 

  • Palmer ME, Ricciardi A (2004) Physical factors affecting the relative abundance of native and invasive amphipods in the St. Lawrence River. Can J Zool 82:1886–1893

    Article  Google Scholar 

  • Phillips AJ, Anderson VL, Robertson EJ, Secombes CJ, van West P (2008) New insights into animal pathogenic oomycetes. Trends Microbiol 16:13–19

    Article  CAS  PubMed  Google Scholar 

  • Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Quiniou SMA, Bigler S, Clem LW, Bly JE (1998) Effects of water temperature on mucous cell distribution in channel catfish epidermis: a factor in winter saprolegniasis. Fish Shellfish Immunol 8:1–11

    Article  Google Scholar 

  • Ramaiah N (2006) A review on fungal diseases of algae, marine fishes, shrimps and corals. Indian J Mar Sci 35:380–387

    Google Scholar 

  • Rondeau B (1993) Qualité des eaux du fleuve Saint-Laurent (1985–1990). Tronçon Cornwall-Québec. Environment Canada, Conservation and Protection, Quebec Region, St. Lawrence Centre, Montreal

  • Ruthig GR (2008) The influence of temperature and spatial distribution on the susceptibility of southern leopard frog eggs to disease. Oecologia 156:895–903

    Article  PubMed  Google Scholar 

  • Sagvik J, Uller T, Stenlund T, Olsson M (2008) Intraspecific variation in resistance of frog eggs to fungal infection. Evol Ecol 22:193–201

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Settle WH, Wilson LT (1990) Invasion by the variegated leafhopper and biotic interactions—parasitism, competition and apparent competition. Ecology 71:1461–1470

    Article  Google Scholar 

  • Söderhäll K, Johansson MW, Smith VJ (1988) Internal defence mechanisms. In: Holdich D, Lowery R (eds) Biology, management and exploitation. Croom Helm Ltd, London, pp 213–235

    Google Scholar 

  • Söderhäll K, Dick MW, Clark G, Furst M, Constantinescu O (1991) Isolation of Saprolegnia parasitica from the crayfish Astacus leptodactylus. Aquaculture 92:121–125

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (2001) Biometry. W.H. Freeman and Co., New York

    Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tompkins DM, White AR, Boots M (2003) Ecological replacement of native red squirrels by invasive greys driven by disease. Ecol Lett 6:189–196

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124:S137–S151

    Article  Google Scholar 

  • Unestam T (1973) Fungal diseases of Crustacea. Rev Med Vet Mycol 8:1–20

    Google Scholar 

  • Vrålstad T, Knutsen AK, Tengs T, Holst-Jensen A (2009) A quantitative TaqMan (R) MGB real-time polymerase chain reaction based assay for detection of the causative agent of crayfish plague Aphanomyces astaci. Vet Microbiol 137:146–155

    Article  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand DH, Sninsky J, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Wolinska J, King KC, Vigneux F, Lively CM (2008) Virulence, cultivating conditions, and phylogenetic analyses of oomycete parasites in Daphnia. Parasitology 135:1667–1678

    Article  CAS  PubMed  Google Scholar 

  • Wolinska J, Giessler S, Koerner H (2009) Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Appl Environ Microbiol 75:7051–7059

    Article  CAS  PubMed  Google Scholar 

  • Zhou JZ, Davey ME, Figueras JB, Rivkina E, Gilichinsky D, Tiedje JM (1997) Phylogenetic diversity of a bacterial community determined from Siberian tundra soil DNA. Microbiology 143:3913–3919

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank A. Derry, N. Gerardo, I. Hebert, M. Lacharité and N. Bayani for helpful assistance and two anonymous reviewers for providing helpful comments on the manuscript. The study was funded by the Canadian Aquatic Invasive Species Network, the Georgia Institute of Technology, and the US National Science Foundation (0827396).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Meghan A. Duffy.

Additional information

Åsa M. Kestrup and Sara H. Thomas contributed equally.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kestrup, Å.M., Thomas, S.H., van Rensburg, K. et al. Differential infection of exotic and native freshwater amphipods by a parasitic water mold in the St. Lawrence River. Biol Invasions 13, 769–779 (2011). https://doi.org/10.1007/s10530-010-9867-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9867-8

Keywords

Navigation