Skip to main content

Advertisement

SpringerLink
Log in

Parasite community similarity in Athabasca River trout-perch (Percopsis omiscomaycus) varies with local-scale land use and sediment hydrocarbons, but not distance or linear gradients

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Parasite communities have been shown to be structured by processes at scales ranging from continental to microhabitat, but few studies have simultaneously considered spatial and environmental variables, measured at different scales, to assess their relative influences on parasite abundance, species richness, and community similarity. Parasite abundance, diversity, and community similarity in Athabasca River trout-perch (Percopsis omiscomaycus) were examined in relation to water quality, substrate profile, metal and organic compound levels in water and sediment, and landscape use patterns at different scales, as well as distance among sites and upstream-downstream position along the river. Although species richness did not differ among sites, there were significant differences in abundance of individual taxa and community structure. We observed a shift from communities dominated by larval trematodes Diplostomum spp. to domination by gill monogeneans Urocleidus baldwini, followed by a reversion further downstream. Variations in the abundance of these taxa and of overall community similarity were strongly correlated with sediment hydrocarbons (alkanes and polycyclic aromatic hydrocarbons (PAHs)) as well as landscape use within 5 km of study sites. No correlations were noted with any other predictors, indicating that parasite populations and communities in this system were likely primarily influenced by habitat level and landscape-scale filters, rather than larger-scale processes such as distance decay or river continuum effects.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson TK, Sukhdeo MVK (2009) Abiotic versus biotic hierarchies in the assembly of parasite populations. Parasitology 137:743–754

    Article  PubMed  Google Scholar 

  • Baldwin RE, Goater CP (2003) Circulation of parasites among fishes from lakes in the Caribou Mountains, Alberta, Canada. J Parasitol 89:215–225

    Article  PubMed  Google Scholar 

  • Beverley-Burton M (1984) Monogenea and Turbellaria. In: Margolis L and Kabata Z (eds) Guide to the parasites of fishes of Canada. Part I. Canadian Special Publication of Fisheries and Aquatic Sciences 74, pp 5–209

  • Bidleman TF (1999) Atmospheric transport and air-surface exchange of pesticides. Water Air Soil Pollut 115:115–166

    Article  CAS  Google Scholar 

  • Blanar CA, Munkittrick KR, Houlahan J, MacLatchy DL, Marcogliese DJ (2009) Pollution and parasitism in aquatic animals: a meta-analysis of effect size. Aquat Toxicol 93:18–28

    Article  CAS  PubMed  Google Scholar 

  • Blanar CA, MacLatchy DL, Kieffer JD, Munkittrick KR (2010) Exposure to a mixture of zinc and copper decreases survival and fecundity of Discocotyle sagittata (Leuckart) parasitizing juvenile Atlantic salmon, Salmo salar L. Bull Environ Contam Toxicol 84:692–697

    Article  CAS  PubMed  Google Scholar 

  • Blanar CA, Marcogliese DJ, Couillard CM (2011) Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitol 58:240–250

    Article  CAS  PubMed  Google Scholar 

  • Blasco-Costa I, Koehler AV, Martin A, Poulin R (2013) Upstream-downstream gradient in infection levels by fish parasites: a common river pattern? Parasitology 140:266–274

    Article  PubMed  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Clarke KR, Gorley RN, Somerfeld PJ, Warwick RM (2014) Change in marine communities: an approach to statistical analysis and interpretation, 3rd edn. PRIMER-E, Plymouth

    Google Scholar 

  • Coggins JR, Tedesco JL, Rupprecht CE (1982) Seasonal changes and overwintering of parasites in the bat, Myotis lucifugus (Le Conte), in a Wisconsin hibernaculum. Am Midl Nat 107:305–315

    Article  Google Scholar 

  • Conly FM, Crosley RW, Headley JV (2002) Characterizing sediment sources and natural hydrocarbon inputs in the lower Athabasca River, Canada. J Environ Eng Sci 1:187–199

    Article  CAS  Google Scholar 

  • Dautremepuits C, Marcogliese DJ, Gendron AD, Fournier M (2008) Gill and head kidney antioxidant processed and innate immune system responses of yellow perch (Perca flavescens) exposed to different contaminants in the St. Lawrence River, Canada. Sci Total Environ 407:1055–1064

    Article  PubMed  Google Scholar 

  • Dechtiar AO (1974) Cleidodiscus baldwini vi. sp. (Monogenoidea: Ancyrocephalinae) from the gills of trout-perch (Percopsis omiscomaycus) of Lake Huron. J Fish Res Board Can 31:163–165

    Article  Google Scholar 

  • Désilets HD, Locke SA, McLaughlin JD, Marcogliese DJ (2013) Community structure of Diplostomum spp. (Digenea: Diplostomidae) in eyes of fish: main determinants and potential interspecific interactions. Int J Parasitol 43:929–939

    Article  PubMed  Google Scholar 

  • Diamant A, Banet A, Paperna I, Westernhagen HV, Broeg K, Kruener G, Koerting W, Zander S (1999) The use of fish metabolic, pathological and parasitological indices in pollution monitoring. II. The Red Sea and Mediterranean. Helgol Mar Res 53:195–208

    Article  Google Scholar 

  • Fausch KD, Togersen CE, Baxter CV, Li HW (2002) Landscapes to riverscapes: bridging the gap between research and conservation of stream fishes. Bioscience 52:483–498

    Article  Google Scholar 

  • Fenton MM, Waters EJ, Pawley SM, Atkinson N, Utting DJ, McKay K (2013) Alberta Geological Survey: surficial geology of Alberta (http://www.ags.gov.ab.ca/publications/abstracts/Map_601.html, accessed October 27, 2014)

  • Gibbons WN, Munkittrick KR, McMaster ME, Taylor WR (1998) Monitoring aquatic environments receiving industrial effluents using small fish species. 2. Comparison between responses of trout-perch (Percopsis omiscomaycus) and white sucker (Catostomus commersoni) downstream of a pulp mill. Environ Toxicol Chem 17:2238–2245

    CAS  Google Scholar 

  • Gibson DI (1996) Trematoda. In: Margolis L, Kabata Z (eds) Guide to the parasites of fishes of Canada. Part IV. Can Spec Pub Fish Aquatic Sci 124: 1–373

  • Guégan JF, Morand S, Poulin R (2005) Are there general laws in parasite community ecology? The emergence of spatial parasitology and epidemiology. In: Thomas F, Renaud JF, Guégan JF (eds) Parasitism and ecosystems. Oxford Biology, Oxford

    Google Scholar 

  • Hatfield Consultants (2009). RAMP technical design and rationale. RAMP1467.1. Retrieved from http://www.ramp-alberta.org/UserFiles/File/RAMP_Design_&_Rationale.pdf

  • Headley JV, Akre C, Conly FM, Peru KM, Dickson LC (2001) Preliminary characterization and source assessment of PAHs in tributary sediments of the Athabasca River, Canada. Environ Forensic 2:335–345

    Article  CAS  Google Scholar 

  • Hechinger RF, Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc Nat Soc Lond B 272:1059–1066

    Article  Google Scholar 

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

    Google Scholar 

  • Holt RD (1999) A biogeographical and landscape perspective on within-host infection dynamics. In: Bell CR, Brylinsky M, Joshnson-Green P (eds) Microbial biosystems: new frontiers. Proceedings of the 8th International Symposium on Microbial Ecology. Canada Society for Microbial Ecology, Halifax

    Google Scholar 

  • Kelly EN, Short JW, Schindler DW, Hodson PV, Ma M, Kwan AK, Fortin BL (2009) Oil sands development contributes polycyclic aromatic compounds to the Athabasca River and its tributaries. Proc Natl Acad Sci U S A 106:22346–22351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan RA, Thulin J (1991) Influence of pollution on parasites of aquatic animals. Adv Parasitol 30:201–238

    Article  CAS  PubMed  Google Scholar 

  • King KC, McLaughlin JD, Boily M, Marcogliese DJ (2010) Effects of agricultural landscape and pesticides on parasitism in native bullfrogs. Biol Conserv 143:302–310

    Article  Google Scholar 

  • Krasnov BR, Shenbrot GI, Kholkhova IS, Stanko M, Morand S, Mouillot D (2014) Assembly rules of ectoparasite communities across scales: combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits. Ecography 37:001–014

    Article  Google Scholar 

  • Kuchta R, Vlčková R, Poddubnaya LG, Gustinelli A, Dzika E, Scholz T (2007) Invalidity of three Palearctic species of Triaenophorus tapeworms (Cestoda: Pseudophyllidea): evidence from morphometric analysis of scolex hooks. Folia Parasitol 54:34–42

    Article  PubMed  Google Scholar 

  • Lafferty KD (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitol Today 13:251–255

    Article  CAS  PubMed  Google Scholar 

  • Landsberg JH, Blakesley BA, Reese RO, McRae G, Forstchen PR (1998) Parasites of fish as indicators of environmental stress. Environ Monit Assess 51:211–232

    Article  Google Scholar 

  • Lenat DR, Penrose DL (1996) History of the EPT taxa richness metric. Bull N Am Benthol Soc 13:305–306

    Google Scholar 

  • Locke SA, McLaughlin JD, Dayanandan S, Marcogliese DJ (2010) Diversity, specificity and evidence of hybridization in Diplostomum spp. metacercariae in freshwater fishes is revealed by DNA barcodes and ITS sequences. Int J Parasitol 40:333–343

    Article  CAS  PubMed  Google Scholar 

  • Locke SA, Levy MS, Marcogliese DJ, Ackerman S, McLaughlin JD (2012) The decay of parasite community similarity in ring‐billed gulls Larus delawarensis and other hosts. Ecography 35:530–538

    Article  Google Scholar 

  • Locke SA, McLaughlin JD, Marcogliese DJ (2013) Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122:73–83

    Article  Google Scholar 

  • MacKenzie K (1999) Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Mar Pollut Bull 38:955–959

    Article  CAS  Google Scholar 

  • MacKenzie K, Williams HH, Williams B, McVicar AH, Siddall R (1995) Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv Parasitol 35:85–144

    Article  CAS  PubMed  Google Scholar 

  • Marcogliese DJ (2005) Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 35:705–716

    Article  PubMed  Google Scholar 

  • Marcogliese DJ, Compagna S, Bergeron E, McLaughlin JD (2001) Population biology of eyeflukes in fish from a large fluvial ecosystem: the importance of gulls and habitat characteristics. Can J Zool 79:1102–1113

    Article  Google Scholar 

  • Marcogliese DJ, Gendron AD, Plante C, Fournier M, Cyr D (2006) Parasites of spottail shiners (Notropis hudsonius) in the St. Lawrence River: effects of municipal effluents and habitat. Can J Zool 84:1461–1481

    Article  CAS  Google Scholar 

  • Marcogliese DJ, Gendron AD, Cone DK (2009) Impact of municipal effluents and hydrological regime on myxozoan parasite communities of fish. Int J Parasitol 39:1345–1351

    Article  CAS  PubMed  Google Scholar 

  • Margolis L, Arthur JR (1979) Synopsis of the parasites of fishes of Canada. Bull Fish Res Board Can 179:1–269

    Google Scholar 

  • McDonald TE, Margolis L (1995) Synopsis of the parasites of fishes of Canada: supplement (1978–1993). Can Spec Publ Fish Aquat Sci 122:1–265

    Google Scholar 

  • Moravec F (1994) Parasitic nematodes of freshwater fishes of Europe. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Nelson PA, Dick TA (2002) Factors shaping the parasite communities of trout-perch, Percopsis omiscomaycus Walbaum (Osteichthyes: Percopsidae), and the importance of scale. Can J Zool 80:1986–1999

    Article  Google Scholar 

  • Nelson PA, Choudhury A, Dick TA (1997) Crepidostomum percopsisi n. sp. (Digenea: Allocreadidae) from the trout perch (Percopsis omiscomaycus) of Dauphin Lake, Canada. J Parasitol 83:1157–1160

    Article  CAS  PubMed  Google Scholar 

  • Nelson PA, Johnson MW, Cott PA (2010) Parasites and diet of trout-perch (Percopsis omiscomaycus) from Northwest Territories, Canada, with comments on the range of Crepidostomum percopsisi Nelson, Chudhury and Dick 1997. Comp Parasitol 77:94–99

    Article  Google Scholar 

  • NLET (2008) SOP 2003—standard operating procedure for the analysis of dissolved, extractable and total trace metals by “direct aspiration” or “in bottle digestion” using inductively coupled plasma-sector field mass spectrometry (ICP-SFMS). Environment Canada, Burlington

    Google Scholar 

  • Petts GE (2009) Rivers: dynamic components of catchment ecosystems. In: Calow PP, Petts GE (eds) Rivers handbook: the science and management of river environments. Blackwell Science Ltd, Oxford

    Google Scholar 

  • Poff NL (1997) Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. J North Am Benthol Soc 16:391–409

    Article  Google Scholar 

  • Poulin R (1992) Toxic pollution and parasitism in freshwater fish. Parasitol Today 8:58–61

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (2001) Interactions between species and the structure of helminth communities. Parasitology 122(S1):S3–S11

    Article  PubMed  Google Scholar 

  • Poulin R (2003) The decay of similarity with geographical distance in parasite communities of vertebrate hosts. J Biogeogr 30:1609–1615

    Article  Google Scholar 

  • Poulin R, Morand S (1999) Geographical distance and the similarity among parasite communities of conspecific host populations. Parasitology 119:369–374

    Article  PubMed  Google Scholar 

  • Poulin R, Blanar CA, Thieltges D, Marcogliese DJ (2011) The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34:540–551

    Article  Google Scholar 

  • Reiczigel J (2003) Confidence intervals for the binomial parameter: some new considerations. Stat Med 22:611–621

    Article  PubMed  Google Scholar 

  • Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86:228–232

    Article  PubMed  Google Scholar 

  • Schindler DW (2010) Tar sands need solid science. Nature 468:499–501

    Article  CAS  PubMed  Google Scholar 

  • Schmidt GD (1986) Handbook of tapeworm identification. CRC Press, Boca Raton

    Google Scholar 

  • Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Bulletin 184. Fisheries Research Board of Canada, Ottawa

    Google Scholar 

  • Thieltges DW, Dolch T, Krakau M, Poulin R (2010) Salinity gradient shapes distance decay of similarity among parasite communities in three marine fishes. J Fish Biol 76:1806–1814

    Article  CAS  PubMed  Google Scholar 

  • Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137

    Article  Google Scholar 

  • Vidal-Martinez VM, Pech D, Sures B, Purucker ST, Poulin R (2010) Can parasites really reveal environmental impact? Trends Parasitol 26:44–51

    Article  PubMed  Google Scholar 

  • Wang Z, Yang C, Parrott JL, Frank RA, Yang Y, Brown CE, Hollebone BP, Landriault M, Fieldhouse B, Liu Y, Zhang G, Hewitt LM (2014) Forensic source differentiation of pterogenic, pyrogenic, and biogenic hydrocarbons in Canadian oil sands environmental samples. J Hazard Mater 271:166–177

    Article  CAS  PubMed  Google Scholar 

  • Warburton EM, Kohler SL, Vonhof MJ (2015) Patterns of parasite community dissimilarity: the significant role of land use and lack of distance-decay in a bat helminth system. Oikos. doi:10.1111/oik.02313

    Google Scholar 

Download references

Acknowledgments

We thank François Boudreault for GIS data; Sean Locke for larval digenean identifications; František Moravec for advice on nematode identification; Andrée Gendron and members of the Marcogliese lab for technical assistance; Gerald Tetreault, Jim Bennett, Thomas Clark, Heather Keith, D. Gilroy, R. Neureuther, R. Frank, and C. Talbot for assistance with field collections; and R. Vanderveen, S. Batchelor, and M. Brown for sample distributions to participating laboratories. We are also grateful to Yves de Lafontaine and several anonymous reviewers for their constructive comments.

Author information

Authors and Affiliations

  1. Department of Biology, Halmos College of Natural Sciences and Oceanography, Nova Southeastern University, Davie, FL, 33314, USA

    C. A. Blanar

  2. Aquatic Contaminants Research Division, Water Science and Technology Directorate, Science and Technology Branch, National Water Research Institute, Environment Canada, 867 Lakeshore Road, Burlington, ON, L7S 1A1, Canada

    M. Hewitt, M. McMaster, J. Kirk & W. Norwood

  3. Emergencies Operational Analytical Laboratories and Research Support Division, Water Science and Technology Directorate, Science and Technology Branch, Environment Canada Ottawa, Ottawa, ON, K1A 0H3, Canada

    Z. Wang

  4. Aquatic Contaminants Research Division, Water Science and Technology Directorate, Science and Technology Branch, Saint Lawrence Centre, Environment Canada, 105 McGill, 7th floor, Montréal, Québec, H2Y 2E7, Canada

    D. J. Marcogliese

Authors
  1. C. A. Blanar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Hewitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. McMaster
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Kirk
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Z. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. W. Norwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. J. Marcogliese
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. A. Blanar.

Ethics declarations

Financial support

CAB was supported by a Natural Sciences and Engineering Research Council Visiting Fellowship in a Canadian Government Laboratory. This project was supported by Environment Canada.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Blanar, C.A., Hewitt, M., McMaster, M. et al. Parasite community similarity in Athabasca River trout-perch (Percopsis omiscomaycus) varies with local-scale land use and sediment hydrocarbons, but not distance or linear gradients. Parasitol Res 115, 3853–3866 (2016). https://doi.org/10.1007/s00436-016-5151-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-016-5151-x

Keywords

Search

Navigation