Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-06-16T01:13:43.222Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatiotemporal distributions of intestinal helminths in female lesser scaup Aythya affinis during spring migration from the upper Midwest, USA

Published online by Cambridge University Press:  27 July 2016

J.C. England ,
J.M. Levengood ,
J.M. Osborn ,
A.P. Yetter ,
J.M. Kinsella ,
R.A. Cole ,
C.D. Suski  and
H.M. Hagy
J.C. England*
Affiliation:
Frank C. Bellrose Waterfowl Research Center, Forbes Biological Station, Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Havana, IL 62644, USA
J.M. Levengood
Affiliation:
Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Champaign, Illinois, 61820, USA
J.M. Osborn
Affiliation:
Frank C. Bellrose Waterfowl Research Center, Forbes Biological Station, Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Havana, IL 62644, USA
A.P. Yetter
Affiliation:
Frank C. Bellrose Waterfowl Research Center, Forbes Biological Station, Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Havana, IL 62644, USA
J.M. Kinsella
Affiliation:
HelmWest Laboratory, Missoula, Montana, 59801, USA
R.A. Cole
Affiliation:
United States Geological Survey-National Wildlife Health Center, Madison, Wisconsin, 53711, USA
C.D. Suski
Affiliation:
Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Champaign, Illinois, 61820, USA
H.M. Hagy
Affiliation:
Frank C. Bellrose Waterfowl Research Center, Forbes Biological Station, Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Havana, IL 62644, USA
*
*E-mail: Cengland@illinois.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

We examined the associations between intestinal helminth infracommunity structure and infection parameters and the age, size, and year and region of collection of 130 female lesser scaup (Aythya affinis) during their 2014–2015 spring migrations through the upper Midwest, USA. We identified a total of 647,174 individual helminths from 40 taxa, including 20 trematodes, 14 cestodes, 4 nematodes and 2 acanthocephalans parasitizing lesser scaup within the study area. Lesser scaup were each infected with 2–23 helminth taxa. One digenean, Plenosoma minimum, is reported for the first time in lesser scaup and in the Midwest. Mean trematode abundance and total helminth abundance was significantly less in 2015 than 2014, and we suspect that colder weather late in 2015 impacted the intermediate host fauna and caused the observed differences. Brillouin's species diversity of helminths was greatest in the northernmost region of the study area, which coincides with the range of a non-indigenous snail that indirectly causes annual mortality events of lesser scaup. While host age and size were not determined to be influential factors of helminth infracommunity structure, non-parametric ordination and permutational analysis of co-variance revealed that year and region of collection explained differences in helminth infracommunities. Our results suggest that spatiotemporal variations play an important role in the structure of intestinal helminth infracommunities found in migrating lesser scaup hosts, and may therefore impact host ability to build endogenous reserves at certain stopover locations in the Midwest.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 4 , July 2017 , pp. 479 - 490
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Afton, A.D. & Anderson, M.G. (2001) Declining scaup populations: a retrospective analysis of long-term population and harvest survey data. Journal of Wildlife Management 65, 781–796.Google Scholar
Anderson, M.J., Gorley, R.N. & Clarke, K.R. (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. 218 pp. Plymouth, UK, PRIMER-E Ltd.Google Scholar
Anteau, M.J. & Afton, A.D. (2004) Nutrient reserves of lesser scaup (Aythya affinis) during spring migration in the Mississippi Flyway: a test of the spring condition hypothesis. Auk 121, 917–929.CrossRefGoogle Scholar
Anteau, M.J. & Afton, A.D. (2006) Diet shifts of lesser scaup are consistent with the spring condition hypothesis. Canadian Journal of Zoology 84, 779–786.Google Scholar
Anteau, M.J. & Afton, A.D. (2008) Diets of lesser scaup during spring migration throughout the upper-Midwest are consistent with the spring condition hypothesis. Waterbirds 31, 97–106.Google Scholar
Austin, J.E., Anteau, M.J., Barclay, J.S., Boomer, G.S., Rohwer, F.C. & Slattery, S.M. (2006) Declining scaup populations: reassessment of the issues, hypotheses, and research directions. Consensus Report from Second Scaup Workshop, 17–19 January, Bismarck, North Dakota, USA.Google Scholar
Beals, M.L. (2006) Understanding community structure: a data-driven multivariate approach. Oecologia 150, 484–495.Google Scholar
Bellrose, F.C. (1976) Ducks, geese, and swans of North America. Harrisburg, Stackpole Books.Google Scholar
Bergmame, L., Huffman, J., Cole, R.A., Dayanandan, S., Tkach, V. & McLaughlin, J.D. (2011) Sphaeridiotrema globulus and Sphaeridiotrema pseudoglobulus (Digenea): differentiation based on mtDNA (barcode) and partial LSU-rDNA sequences. Journal of Parasitology 97, 1132–1136.Google Scholar
Brown, S.P., André, J., Ferdy, J. & Godelle, B. (2005) Subverting hosts and diverting ecosystems: an evolutionary modelling perspective. pp. 140–154 in Thomas, F., Renaud, F. & Guégan, J. (Eds) Parasitism and ecosystems. Oxford, Oxford University Press.Google Scholar
Bush, A.O. & Holmes, J.C. (1986a) Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology 64, 142–152.Google Scholar
Bush, A.O. & Holmes, J.C. (1986b) Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64, 132–141.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Clarke, K.R. & Gorley, R.N. (2015) PRIMER v. 7: user manual/tutorial. 300 pp. Plymouth, UK, PRIMER-E Ltd.Google Scholar
Clarke, K.R., Gorley, R.N., Somerfield, P.J. & Warwick, R.M. (2014) Change in marine communities: an approach to statistical analysis and interpretation. 3rd edn. 262 pp. Plymouth, UK, PRIMER-E Ltd.Google Scholar
Cole, R.A. & Friend, M. (1999) Miscellaneous parasitic diseases. pp. 249–258 in Friend, M. & Franson, J.C. (Eds) Field manual of wildlife diseases: general field procedures and diseases of birds. Washington DC, United States Geological Survey.Google Scholar
Crawley, M.J. (2005) Statistics: an introduction using R. 337 pp. West Sussex, Wiley.Google Scholar
Drever, M.C., Clark, R.G., Derksen, C., Slattery, S.M., Toose, P. & Nudds, T.D. (2012) Population vulnerability to climate change linked to timing of breeding in boreal ducks. Global Change Biology 18, 480–492.Google Scholar
Hagy, H.M., Yetter, A.P., Osborn, J.M., Horath, M.M., Hine, C.S., McClain, D., Walter, K., Gilbert, A., Benson, T.J., Fox, J. & Ward, M.P. (2015) Illinois waterfowl surveys and investigations. W-43-R-62. Final Annual Report (FY15). INHS Technical Report 2015 (39). 198 pp. Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Champaign, Illinois.Google Scholar
Hanssen, S.A., Hasselquist, D., Folstad, I. & Erikstad, K.E. (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings of the Royal Society of London B 271, 925–930.Google Scholar
Hechinger, R.F. & Lafferty, K.D. (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B 272, 1059–1066.CrossRefGoogle ScholarPubMed
Herrmann, K.K. & Sorensen, R.E. (2011) Differences in natural infections of two mortality-related trematodes in lesser scaup and American coot. Journal of Parasitology 97, 555–558.Google Scholar
Hoeve, J. & Scott, M.E. (1988) Ecological studies on Cyathocotyle bushiensis (Digenea) and Sphaeridiotrema globulus (Digenea), possible pathogens of dabbling ducks in southern Quebec. Journal of Wildlife Diseases 24, 407–421.Google Scholar
Hollmén, T., Lehtonen, J.T., Sankari, S., Soveri, T. & Hario, M. (1999) An experimental study on the effects of polymorphiasis in common eider ducklings. Journal of Wildlife Diseases 35, 466–473.Google Scholar
Holt, R. & Boulinier, T. (2005) Ecosystems and parasitism: the spatial dimension. pp. 68–84 in Thomas, F., Renaud, F. & Guégan, J. (Eds) Parasitism and ecosystems. Oxford, Oxford University Press.Google Scholar
Huffman, J. (2008) Trematodes. pp. 225–245 in Atkinson, C.T., Thomas, N.J. & Hunter, D.B. (Eds) Parasitic diseases of wild birds. Ames, Wiley-Blackwell.Google Scholar
Kahlil, L.F., Jones, A. & Bray, R.A. (1994) Keys to the cestode parasites of vertebrates. 751 pp. Wallingford, CAB International.Google Scholar
Kanarek, G. & Zaleśny, G. (2013) Extrinsic- and intrinsic-dependent variation in component communities and patterns of aggregations in helminth parasites of great cormorant (Phalacrocorax carbo) from N.E. Poland. Parasitology Research 113, 837–850.CrossRefGoogle ScholarPubMed
Karatayev, A.Y., Mastitsky, S.E., Burlakova, L.E., Karatayev, V.A., Hajduk, M.M. & Conn, D.B. (2012) Exotic mollusks in the Great Lakes host epizootically important trematodes. Journal of Shellfish Research 31, 885–894.Google Scholar
Lafferty, K.D. (2010) Interacting parasites. Science 330, 187–188.Google Scholar
Lafferty, K.D. & Kuris, A.M. (2005) Parasitism and environmental disturbances. pp. 113–123 in Thomas, F., Renaud, F. & Guégan, J. (Eds) Parasitism and ecosystems. Oxford, Oxford University Press.Google Scholar
Lafferty, K.D., Dobson, A.P. & Kuris, A.M. (2006) Parasites dominate food web links. PNAS 103, 11211–11216.Google Scholar
Mayer, K.A., Dailey, M.D. & Miller, M.A. (2003) Helminth parasites of the southern sea otter Enhydra lutris nereis in central California: abundance, distribution and pathology. Diseases of Aquatic Organisms 53, 77–88.CrossRefGoogle ScholarPubMed
McDonald, M.E. (1974) Key to nematodes reported in waterfowl. Resource Publication 122. Washington DC, United States Department of the Interior.Google Scholar
McDonald, M.E. (1981) Key to trematodes reported in waterfowl. Resource Publication 142. Washington DC, United States Department of the Interior.Google Scholar
McDonald, M.E. (1988) Key to acanthocephala reported in waterfowl. Resource Publication 173. Washington DC, United States Department of the Interior.Google Scholar
McLaughlin, J.D. (2008) Cestodes. pp. 261–276 in Atkinson, C.T., Thomas, N.J. & Hunter, D.B. (Eds) Parasitic diseases of wild birds. Ames, Wiley-Blackwell.Google Scholar
McLaughlin, J.D. & Burt, M.D.B. (1973) Changes in the cestode fauna of the black duck, Anas rubripes (Brewster). Canadian Journal of Zoology 51, 1001–1006.Google Scholar
Mills, E.L., Leach, J.H., Carlton, J.T. & Secor, C. (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. Journal of Great Lakes Research 19, 1–54.Google Scholar
Møller, A.P. (2005) Parasitism and the regulation of host populations. pp. 43–53 in Thomas, F., Renaud, F. & Guégan, J. (Eds) Parasitism and ecosystems. Oxford, Oxford University Press.Google Scholar
NOAA (National Oceanic and Atmospheric Administration). (2015) National temperature and precipitation maps. Available online at http://www.ncdc.noaa.gov/temp-and-precip/asos/avgtemp.dfn/dot/monthly/201403 (accessed December 2015).Google Scholar
Pedersen, A.B. & Fenton, A. (2006) Emphasizing the ecology in parasite community ecology. TRENDS in Ecology and Evolution 22, 133–139.Google Scholar
Pritchard, M.H. (1982) The collection and preservation of animal parasites. 141 pp. Lincoln, University of Nebraska Press.Google Scholar
Reiczigel, J. (2003) Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.Google Scholar
Reiczigel, J. & Ròzsa, L. (2005) Quantitative parasitology 3.0. Available online at http://www.zoologia.hu/qp/qp.html (accessed September 2015).Google Scholar
Ròzsa, L., Reiczigel, J. & Majoros, G. (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.CrossRefGoogle ScholarPubMed
Sandland, G.J., Gillis, R., Haro, R.J. & Peirce, J.P. (2014) Infection patterns in invasive and native snail hosts exposed to a parasite associated with waterfowl mortality in the upper Mississippi River, USA. Journal of Wildlife Diseases 50, 125–129.Google Scholar
Santoro, M., Badillo, F.J., Mattiucci, S., Nascetti, G., Bentivegna, F., Insacco, G., Travaglini, A., Paoletti, M., Kinsella, J.M., Tomás, J., Raga, J.A. & Aznar, F.J. (2010) Helminth communities of loggerhead turtles (Caretta caretta) from Central and Western Mediterranean Sea: the importance of host's ontogeny. Parasitology International 59, 367–375.Google Scholar
Santoro, M., Aznar, F.J., Mattiucci, S., Kinsella, J.M., Pellegrino, F., Cipriani, P. & Nascetti, G. (2012) Parasite assemblages in the western whip snake Hierophis viridiflavus carbonarius (Colubridae) from southern Italy. Journal of Helminthology 87, 277–285.Google Scholar
Sauer, J.S., Cole, R.A. & Nissen, J.M. (2007) Finding the exotic faucet snail (Bithynia tentaculata): investigation of waterbird die-offs on the Upper Mississippi River National Wildlife and Fish Refuge. Open File Report 2007–1065. Washington DC, United States Geological Survey.Google Scholar
Schmidt, G.D. (1986) Handbook of tapeworm identification. 675 pp. Boca Raton, CRC Press.Google Scholar
Sepúlveda, M.S. & Kinsella, J.M. (2013) Helminth collection and identification from wildlife. Journal of Visualized Experiments 82, doi: 10.3791/51000. Available at website http://www.ncbi.nlm.nih.gov/pubmed/24378960 (accessed May 2014).Google Scholar
Shutler, D., Alisauskas, R.T. & McLaughlin, J.D. (2012) Associations between body composition and helminths of lesser snow geese during winter and spring migration. International Journal for Parasitology 42, 755–760.CrossRefGoogle Scholar
Skerratt, L.F., Franson, J.C., Meteyer, C.U. & Hollmén, T.E. (2005) Causes of mortality in sea ducks (mergini) necropsied at the USGS-National Wildlife Health Center. Waterbirds 28, 193–207.Google Scholar
Stafford, J.D., Janke, A.K., Pearse, A.T., Fox, A.D., Elmberg, J., Straub, J.N., Eicholz, M.W. & Arzel, C. (2014) Spring migration of waterfowl in the northern hemisphere: a conservation perspective. Wildfowl 4, 70–85.Google Scholar
Trauger, D.L. (1974) Eye color of female lesser scaup in relation to age. Auk 91, 243–254.Google Scholar
USFWS (United States Fish and Wildlife Service). (2015) Waterfowl populations status, 2015. Washington DC, United States Department of the Interior.Google Scholar
Viney, M.E. & Lok, J.B. (2007) Strongyloides spp . pp. 1–15 in Hodgkin, J. & Anderson, P. (Eds) Worm book. Available at website http://www.wormbook.org/chapters/www_genomesStrongyloides/genomesStrongyloides.html#bib66 (accessed November 2015).Google Scholar
Wallace, B.M. & Pence, D.B. (1986) Population dynamics of the helminth community from migrating blue-winged teal: loss of helminths without replacement on the wintering grounds. Canadian Journal of Zoology 64, 1765–1773.CrossRefGoogle Scholar
Wobeser, G.A. (1974) Renal coccidiosis in mallard and pintail ducks. Journal of Wildlife Diseases 10, 249–255.CrossRefGoogle ScholarPubMed
Wobeser, G.A. (2008) Parasitism: costs and effects. pp. 3–9 in Atkinson, C.T., Thomas, N.J. & Hunter, D.B. (Eds) Parasitic diseases of wild birds. Ames, Wiley-Blackwell.Google Scholar
Yabsley, M.J. (2008) Capillarid nematodes. pp. 463–497 in Atkinson, C.T., Thomas, N.J. & Hunter, D.B. (Eds) Parasitic diseases of wild birds. Ames, Wiley-Blackwell.Google Scholar
Zar, J.H. (2010) Biostatistical analysis. 5th edn. 960 pp. Old Tappan, Pearson.Google Scholar
Supplementary material: File

England supplementary material

Table S1

Download England supplementary material(File)
File 28.4 KB

England supplementary material

Video V1

Download England supplementary material(Video)
Video 12.5 MB