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Associations of intestinal helminth infections with health parameters of spring-migrating female lesser scaup (Aythya affinis) in the upper Midwest, USA


Thousands of lesser scaup (Aythya affinis) die during spring and fall migrations through the upper Midwest, USA, from infections with Cyathocotyle bushiensis and Sphaeridiotrema spp. (Class: Trematoda) after ingesting infected intermediate hosts, such as non-native faucet snails (Bithynia tentaculata). The lesser scaup is a species of conservation concern and is highly susceptible to these infections. We collected female lesser scaup from spring migratory stopover locations throughout Illinois and Wisconsin and assessed biochemical and morphological indicators of health in relation to intestinal helminth loads. Helminth species diversity, total trematode abundance, and the infection intensities of the trematodes C. bushiensis and Sphaeridiotrema spp. were associated with percent body fat, blood metabolites, hematological measures, and an index of foraging habitat quality. Helminth diversity was negatively associated with percent body fat, albumin concentrations, and monocytes, whereas glucose concentrations displayed a slight, positive association. Total trematode abundance was negatively associated with blood concentrations of non-esterified fatty acids and albumin. Infections of C. bushiensis were positively related to basophil levels, whereas Sphaeridiotrema spp. infection intensity was negatively associated with packed cell volume and foraging habitat quality. Thus, commonly measured health metrics may indicate intestinal parasite infections and help waterfowl managers understand overall habitat quality. Intestinal parasitic loads offer another plausible mechanism underlying the spring condition hypothesis.

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  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

  2. Afton AD, Ankney CD (1991) Nutrient-reserve dynamics of breeding lesser scaup: a test of competing hypotheses. Condor 93:89–97

  3. Anderson DR (2010) Model based inference in the life sciences: a primer on evidence. Springer Science+Business Media LLC, New York, New York, p 184

  4. Anteau MJ, Afton AD (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

  5. Anteau MJ, Afton AD (2008a) Diets of lesser scaup during spring migration throughout the upper-Midwest are consistent with the spring condition hypothesis. Waterbirds 31:97–106

  6. Anteau MJ, Afton AD (2008b) Using plasma-lipid metabolites to index changes in lipid reserves of free-living lesser scaup Aythya affinis. Auk 125:354–357

  7. Anteau MJ, Afton AD (2011) Lipid catabolism of invertebrate predator indicates widespread wetland ecosystem degradation. Plods ONE 6:e16029. https://doi.org/10.1371/journal.pone.0016029. http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0016029. Accessed September 2015

  8. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178

  9. Austin JE, Anteau MJ, Barclay JS, Boomer GS, Rohwer FC, Slattery SM (2006) Declining scaup populations: reassessment of the issues hypotheses and research directions. Consensus report from second scaup workshop 17–19 January. North Dakota, Bismarck, p 7

  10. Bellrose FC (1976) Ducks, geese, and swans of North America. Stackpole Books, Harrisburg, Pennsylvania, p 543

  11. Bergmame L, Huffman J, Cole RA, Dayanandan S, Tkach V, McLaughlin JD (2011) Sphaeridiotrema globulus and Sphaeridiotrema pseudoglobulus (Digenea): differentiation based on mtDNA (barcode) and partial LSU-rDNA sequences. J Parasitol 97:1132–1136

  12. Bogitsh BJ, Carter CE, Oeltmann TN (2013) Human parasitology, 4th edn. Academic Press, Oxford, p 430

  13. Brown SP, André J, Ferdy J, Godelle B (2005) Subverting hosts and diverting ecosystems: an evolutionary modelling perspective. In: Thomas F, Renaud F, Guégan J (eds) Parasitism and Ecosystems. Oxford University Press, Oxford, England, pp 140–154

  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York, New York, p 488

  15. Burnham KP, Anderson DR, Huyvaert KP (2010) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35

  16. Bush AO, Holmes JC (1986) Intestinal helminths of lesser scaup ducks: patterns of association. Can J Zool 64:132–141

  17. 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

  18. Chiavacci SJ, Ward MP, Benson TJ (2015) Why fledge early in the day? Examining the role of predation risk in explaining fledging behavior. Behav Ecol Sociobiol 26:593–600

  19. Cole RA (2001) Exotic parasite causes large scale mortality in American coots. National Wildlife Health Center Report. United States Geological Survey, Washington DC

  20. Cole RA, Franson JC (2006) Recurring waterbird mortalities of unusual etiologies. In: Boere GC, Galbraith CA, Stroud DA (eds) Waterbirds around the world. The Stationery Office, Edinburgh, pp 439–440

  21. Cole RA, Friend M (1999) Miscellaneous parasitic diseases. In: Friend M, Franson JC (eds) Field manual of wildlife diseases: general field procedures and diseases of birds. United States Geological Survey, Washington DC, pp 249–258

  22. DeVink JMA, Clark RG, Slattery SM, Scheuhammer TM (2008) Effects of dietary selenium on reproduction and body mass of captive lesser scaup. Environ Toxicol Chem 27:471–477

  23. Drever MC, Clark RG, Derksen C, Slattery SM, Toose P, Nudds TD (2012) Population vulnerability to climate change linked to timing of breeding in boreal ducks. Glob Chang Biol 18:480–492

  24. England JC (2016) Intestinal helminth infections, distributions, and associations with health parameters of spring-migrating female lesser scaup in the upper Midwest. MSc Thesis, University of Illinois, Urbana, Illinois, p 128

  25. England JC, Levengood JM, Osborn JM, Yetter AP, Kinsella JM, Cole RA, Suski CD, Hagy HM (2017) Spatiotemporal distributions of intestinal helminths in female lesser scaup Aythya affinis during spring migration from the upper Midwest, USA. J Helminthol 91:479–490

  26. Erasmus DA, Öhman C (1963) The structure and function of the adhesive organ in strigeid trematodes. Ann N Y Acad Sci 113:7–35

  27. Friend M, Franson JC (1999) Field manual of wildlife diseases: general field procedures and diseases of birds. United States Geological Survey, Washington DC, p 426

  28. Gagnon C, Scott ME, McLaughlin JD (1993) Gross lesions and hematological changes in domesticated mallard ducklings experimentally infected with Cyathocotyle bushiensis (Digenea). J Parasitol 79:757–762

  29. Hagy HM, Linz GM, Bleier WJ (2010) Wildlife conservation sunflower plots and croplands as fall habitat for migratory birds. Am Midl Nat 164:119–135

  30. Hagy HM, Yetter AP, Osborn JM, Horath MM, Hine CS, McClain D, Walter K, Gilbert A, Benson TJ, Fox J, Ward MP. 2015. Illinois waterfowl surveys and investigations. W-43-R-62. Final Annual Report (FY15). INHS technical report 2015 (39), p 198

  31. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc R Soc Lond B 271:925–930

  32. Harman WN (1968) Replacement of pleurocerids by Bithynia in polluted waters of Central New York. Nautilus 81:77–83

  33. Harr KE (2006) Diagnostic value of biochemistry. In: Harrison GJ, Lightfoot TL (eds) Clinical Avian Medicine, vol 2. Spix Publishing Inc, Palm Beach, Florida, pp 611–630

  34. Harris DJ (2009) Clinical tests. In: Tully TN, Dorrestein GM, Jones AK, Sooper JE, Saunders WB (eds) Handbook of Avian Medicine, 2nd edn. Saunder Ltd, Edinburgh, pp 77–84

  35. 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

  36. Hollmén T, Franson JC, Hario M, Sankari S, Kilpi M, Lindström K (2001) Use of serum biochemistry to evaluate nutritional status and health of incubating common eiders (Somateria mollissima) in Finland. Physiol Biochem Zool 74:333–342

  37. Hoste H (2001) Adaptive physiological processes in the host during gastrointestinal parasitism. Int J Parasitol 31:231–244

  38. Hudelson KS, Hudelson PM (2006) Endocrine system. In: Harrison GJ, Lightfoot TL (eds) Clinical Avian Medicine. Spiz Publishing, Palm Beach, pp 541–557

  39. Hudson PJ (1986) The effects of a parasitic nematode on the breeding production of red grouse. J Anim Ecol 55:85–94

  40. Hudson PJ, Dobson AP (1990) The direct and indirect effects of the caecal nematode Trichostrongylus tenuis on red grouse. In: Loye JE, Zuk M (eds) Bird–parasite Interactions: Ecology Evolution and Behaviour. Oxford University Press, Oxford, pp 49–68

  41. Hudson PJ, Dobson AP, Newborn D (1999) Population cycles and parasitism. Science 282:2256–2258

  42. Huffman JE (2008) Trematodes. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic Diseases of Wild Birds. Wiley-Blackwell, Ames, Iowa, pp 225–245

  43. Krams I, Vrublevska J, Cirule D, Kivleniece I, Krama T, Rantala MJ, Sild E, Horak P (2012) Heterophil/lymphocyte ratios predict the magnitude of humoral immune response to a novel antigen in great tits Parus major. Comp Biochem Physiol A Mol Integr Physiol 161:422–428

  44. Lack D (1954) The natural regulation of animal numbers. Oxford University Press, Oxford, p 343

  45. Lafferty KD, Kuris AM (2005) Parasitism and environmental disturbances. In: Thomas F, Renaud F, Guégan J (eds) Parasitism and Ecosystems. Oxford University Press, Oxford, pp 113–123

  46. Lyons TP, Miller JR, Debinski DM, Engle DM (2015) Predator identity influences the effect of habitat management on nest predation. Ecol Appl 25:1596–1605

  47. Maxwell MH (1993) Avian blood leucocyte response to stress. Worlds Poult Sci J 43:190–207

  48. Maxwell MH, Roberston GW (1995) The avian basophilic leukocyte. Worlds Poult Sci J 51:307–325

  49. McDonald ME (1969) Catalogue of Helminths of Waterfowl (Anatidae), Special scientific report-wildlife no. 126. United States Department of the Interior, Washington DC, p 692

  50. McDonald ME (1974) Key to Nematodes Reported in Waterfowl, Resource publication 122. United States Department of the Interior, Washington DC, p 44

  51. McDonald ME (1981) Key to Trematodes Reported in Waterfowl, Resource publication 142. United States Department of the Interior, Washington DC, p 156

  52. McDonald ME (1988) Key to Acanthocephala Reported in Waterfowl, Resource publication 173. United States Department of the Interior, Washington DC, p 45

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

  54. McLaughlin JD (2008) Cestodes. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic Diseases of Wild Birds. Wiley-Blackwell, Ames, Iowa, pp 261–276

  55. Novakofski JS, Park S, Bechtel PJ, McKeith FK (1989) Composition of cooked pork chops: effects of removing subcutaneous fat before cooking. J Food Sci 54:15–17

  56. Roscoe DE, Huffman JE (1982) Trematode (Sphaeridiotrema globulus) induced ulcerative hemorrhagic enteritis in wild mute swans (Cygnus olor). Avian Dis 26:214–224

  57. 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

  58. 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. United States Geological Survey, open file report 2007–1065, Reston, Virginia, pp. 3

  59. Sepúlveda MS, Spalding MG, Kinsella JM, Bjork RD, McLaughlin JD (1994) Helminths of the roseate spoonbill Ajaia ajaja in southern Florida. J Helminthol Soc Wash 61:179–189

  60. Sepúlveda MS, Kinsella JM (2013) Helminth collection and identification from wildlife. J Vis Exp 82: doi: 103791/51000, http://www.ncbinlmnihgov/pubmed/24378960. Accessed May 2014

  61. Schmidt GD (1986) Handbook of tapeworm identification. CRC Press Inc., Boca Raton, Florida, p 675

  62. Shutler D, Alisauskas RT, McLaughlin JD (2012) Associations between body composition and helminths of lesser snow geese during winter and spring migration. Int J Parasitol 42:755–760

  63. Stafford JD, Janke AK, Anteau MJ, Pearse AT, Fox AD, Elmberg J, Straub JN, Eichholz MW, Arzel C (2014) Spring migration of waterfowl in the northern hemisphere: a conservation perspective. Wildfowl Special Issue 4:70–85

  64. Strand KA, Chipps SR, Kahara SN, Higgins KF, Vaa S (2008) Patterns of prey use by lesser scaup Aythya affinis Aves and diet overlap with fishes during spring migration. Hydrobiologia 598:389–398

  65. Straub JN, Gates RJ, Schultheis RD, Yerkes T, Coluccy JM, Stafford JD (2012) Wetland food resources for spring-migrating ducks in the upper Mississippi rivers and Great Lakes region. J Wildl Manag 76:768–777

  66. Strayer DL, Caraco NF, Cole JJ, Findlay S, Pace ML (1999) Transformation of freshwater ecosystems by bivalves: a case study of zebra mussels in the Hudson River. J BioScience 49:19–27

  67. Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Today 15:311–313

  68. Tompkins DM, Dobson AP, Arneberg P, Begon ME, Cattadori IM, Greenman JV, Heesterbeek AP, Hudson PJ, Newborn D, Pugliese A, Rizzoli AP, Rosá R, Rosso F, Wilson K (2001) Parasites and host population dynamics. In: Hudson PJ, Rizzoli AP, Grenfell BT, Heesterbeek AP, Dobson AP (eds) The Ecology of Wildlife Diseases. Oxford University Press, Oxford, pp 45–62

  69. United States Fish and Wildlife Service (2017) Waterfowl populations status 2017. United States Department of the Interior, Washington DC, p 74

  70. Vandegrift KJ, Raffel TR, Hudson PJ (2008) Parasites prevent summer breeding in white-footed mice, Peromyscus leucopus. Ecology 89:2251–2258

  71. Vest JL (2002) Body mass and gastrointestinal parasites of lesser scaup (Aythya affinis) in the Mississippi Flyway. MSc Thesis, Mississippi State University, Starkville, Mississippi, p 85

  72. Vest JL, Kaminski RM, Afton AD, Vilella FJ (2006) Body mass of lesser scaup during fall and winter in the Mississippi Flyway. J Wildl Manag 70:1789–1795

  73. Vinkler M, Schnitzer J, Munclinger P, Votypka J, Albrecth T (2010) Haematological health assessment in passerine with extremely high proportion of basophiles in peripheral blood. J Ornithol 151:841–849

  74. Wildlife Health Information Sharing Partnership Event Reporting System (2017) Accessed 16 November 2017. <http://www.nwhc.usgs.gov/whispers/>

  75. Wobeser GA (2008) Parasitism: costs and effects. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic Diseases of Wild Birds. Wiley-Blackwell, Ames, Iowa, pp 3–9

  76. Zakeri A (2017) Helminth induced apoptosis: a silent strategy for immunosuppression. Parasitology 144:1663–1676

  77. Zar JH (2010) Biostatistical analysis, 5th edn. Pearson, Old Tappan, New Jersey, p 96

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The authors thank the many technicians, personnel, and other assistants of the Forbes Biological Station for specimen collection efforts; the USGS National Wildlife Health Center, HelmWest Laboratory, and University of Tennessee College of Veterinary Medicine Parasitology Laboratory for the assistance in identifying parasites and other in-kind contributions; the University of Illinois at Urbana-Champaign Meat Science Laboratory and College of Veterinary Medicine Clinical Pathology Laboratory for specimen processing and biochemical analyses; and the Illinois Department of Natural Resources, the US Fish and Wildlife Service, the Nature Conservancy, and many private landowners for providing in-kind support and access to collection sites. We thank T. Lyons for the unyielding analytical support and advice.


For funding, we thank the Illinois Department of Natural Resources through the Federal Aid in Wildlife Restoration Program (W-43-R-61&62; W-176-R-1&2), the US Fish and Wildlife Service through the Flex Fund Grant Program of the Upper Mississippi River and Great Lakes Region Joint Venture (F13AP00229), and the University of Illinois at Urbana-Champaign’s Illinois Natural History Survey Department of Natural Resources and Environmental Sciences.

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Correspondence to J. Conner England.

Ethics declarations

All procedures were approved by the Institutional Animal Care and Use Committee at the University of Illinois (protocol nos. 14295 and 11,229), the US Fish and Wildlife Service (MB145466–1), Illinois Department of Natural Resources (NH14.4071, NH15.4071, SS14-02, and SS15-11), and Wisconsin Department of Natural Resources (SRL-SOD-005-2013).

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The authors declare that they have no conflict of interest.

Statement of interest

Any opinions, findings and conclusions or recommendations expressed in this report are those of the authors and do not necessarily reflect the views of the US Fish and Wildlife Service, US Geological Survey, Bureau of Land Management, Illinois Natural History Survey, Illinois Department of Natural Resources, or the University of Illinois. Use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government.

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Conner England, J., Levengood, J.M., Osborn, J.M. et al. Associations of intestinal helminth infections with health parameters of spring-migrating female lesser scaup (Aythya affinis) in the upper Midwest, USA. Parasitol Res 117, 1877–1890 (2018). https://doi.org/10.1007/s00436-018-5879-6

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  • Cyathocotyle bushiensis
  • Helminth
  • Scaup
  • Sphaeridiotrema
  • Spring condition hypothesis