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The influence of geographical location, host maturity and sex on intestinal helminth communities of the double-crested cormorant Phalacrocorax auritus from the eastern United States

Published online by Cambridge University Press:  28 September 2016

K.L. Sheehan ,
K.C. Hanson-Dorr ,
B.S. Dorr ,
G.K. Yarrow  and
R.J. Johnson
K.L. Sheehan*
Affiliation:
Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive # 0218 La Jolla CA, 92093USA Department of Forestry and Environmental Conservation, Clemson University, Clemson, SC 29634-001USA
K.C. Hanson-Dorr
Affiliation:
US Department of Agriculture, Wildlife Services, National Wildlife Research Center, PO Box 6099, Mississippi State, MS 39762USA
B.S. Dorr
Affiliation:
US Department of Agriculture, Wildlife Services, National Wildlife Research Center, PO Box 6099, Mississippi State, MS 39762USA
G.K. Yarrow
Affiliation:
Department of Forestry and Environmental Conservation, Clemson University, Clemson, SC 29634-001USA
R.J. Johnson
Affiliation:
Department of Forestry and Environmental Conservation, Clemson University, Clemson, SC 29634-001USA
*
*E-mail: klsheehan@ucsd.edu
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Abstract

Here the intestinal helminth infracommunities of 218 double-crested cormorants (Phalacrocorax auritus) from 11 locations in Alabama, Minnesota, Mississippi and Vermont are documented. Trematode infections were present in 98% of hosts; 65% of cormorants carried cestode infections, 4% were infected with acanthocephalans and 66% had nematode intestinal parasites. Parasite infracommunities of hosts collected on wintering grounds had higher richness and diversity than did birds collected on breeding grounds. Differences in parasite richness and diversity between male and female P. auritus were also detected, but not between immature and mature bird hosts. Parasite intensity did not differ by sex, maturity, or between breeding and wintering season. The most common parasite was Drepanocephalus auritus (spathans), which is recognized as a disease agent that negatively impacts the catfish aquaculture industry in the US. Echinochasmus sp. in double-crested cormorants is documented for the first time in the United States. We suggest that the differences observed among parasite infracommunities could be associated with the foraging distances travelled by P. auritus during breeding and wintering seasons, which is limited by allocation of parental care during the breeding season.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 5 , September 2017 , pp. 561 - 568
Creative Commons
This is a work of the U.S. Government and is not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2016

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References

Anderson, C.D., Roby, D.D. & Collis, K. (2004) Foraging patterns of male and female Double-crested Cormorants nesting in the Columbia River estuary. Waterbirds 27, 155–160.CrossRefGoogle Scholar
Arnold, J.G. Jr (1934) Some trematodes of the common bullhead Ameiurus nebulosus (Le Sueur). Transactions of the American Microscopical Society 53, 267–276.Google Scholar
Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. & White, J.S.S. (2008) Generalized linear mixes models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.CrossRefGoogle Scholar
Bush, A.O., Heard, R.W. & Overstreet, R.M. (1993) Intermediate hosts as source communities. Canadian Journal of Zoology 71, 1358–1363.CrossRefGoogle 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
Campo, J.J., Thompson, B.C., Barron, J.C., Telfair, R.C. III, Durocher, P. & Gutreuter, S. (1993) Diet of Double-crested Cormorants wintering in Texas. Journal of Field Ornithology 64, 135–144.Google Scholar
Carney, J.P. & Dick, T.A. (2000) Helminth communities of yellow perch (Perca flavescens (Mitchill)): determinants of pattern. Canadian Journal of Zoology 78, 538–555.CrossRefGoogle Scholar
Casaux, R., Favero, M., Silva, P. & Baroni, A. (2001) Sex differences in the diving depths and diet of Antarctic Shags at the South Shetland Islands. Journal of Field Ornithology 72, 22–29.Google Scholar
Chandler, A.C. & Rausch, R. (1984) A contribution to the study of certain avian strigeids (Trematoda). Journal of Parasitology 34, 207–210.CrossRefGoogle Scholar
Coleman, J.T.H. & Richmond, M.E. (2007) Daily foraging patterns of adult Double-crested Cormorants during the breeding season. Waterbirds 30, 189–198.CrossRefGoogle Scholar
Coleman, J.T.H., Richmond, M.E., Rudstam, L.G. & Mattison, P.M. (2005) Foraging location and site fidelity of the Double-crested Cormorant on Oneida Lake, New York. Waterbirds 28, 498–510.Google Scholar
Craig, E.C., King, D.T., Sparks, J.P. & Curtis, P.D. (2016) Aquaculture depredation by Double-crested Cormorants breeding in eastern North America. Journal of Wildlife Management 80, 57–62.Google Scholar
Custer, T.W. & Bunck, C. (1992) Feeding flights of breeding Double-crested Cormorants at two Wisconsin colonies. Journal of Field Ornithology 63, 203–221.Google Scholar
Doffitt, C.M., Pote, L.M. & King, T. (2009) Experimental Bolbophorous damnificus (Digenea: Bolbophoridae) infections in piscivorous birds. Journal of Wildlife Diseases 45, 684–691.Google Scholar
Dorr, B.S., Burger, L.W., Barras, S.C. & Godwin, K. (2012) Double-crested Cormorant distribution on catfish aquaculture in the Yazoo River Basin of Mississippi. Wildlife Society Bulletin 36, 70–77.CrossRefGoogle Scholar
Dorr, B.S., Hatch, J.J. & Weseloh, D.V. (2014 a) Double-crested Cormorant (Phalacrocorax auritus). In Poole, A. (Ed.) The Birds of North America Online. Ithaca: Cornell Lab of Ornithology. Available at http://bna.birds.cornell.edu/bna/species/441 (accessed 4 September 2016).Google Scholar
Dorr, B.S., Hanson-Dorr, K.C., DeVault, T.L., Barras, S.C. & Guillaumet, A. (2014b) Evidence of geographic segregation and density dependent changes in sex ratios in an abundant colonial waterbird. Integrative Zoology 9, 570–582.Google Scholar
Dorr, B.S., Hanson-Dorr, K.C., Barras, S.C. & DeVault, T.L. (2016) Reproductive characteristics of Double-crested Cormorants in the eastern United States: demographic information for an intensely managed species. Waterbirds 39, 81–85.CrossRefGoogle Scholar
Dronen, N.O. (2009) Austrodiplostomum ostrowskiae n. sp. (Digenea: Diplostomidae: Diplostominae) from the Double-crested Cormorant, Phalacrocorax auritus (Phalacrocoridae) from the Galveston, Texas area of the Gulf of Mexico, U.S.A. Comparative Parasitology 76, 34–39.CrossRefGoogle Scholar
Dubois, G. & Mahon, J. (1959) Etude de quelques Trematodes nordamericanis: suivie d'une revision des generes Galactosomum Looss 1899 et Ochetosoma Braun 1901. Bulletin de la Société Neuchateloise des Sciences Naturelles 82, 191–229.Google Scholar
Fenech, A.S., Lochman, S.E. & Radomski, A.A. (2004) Seasonal diets of male and female Double-crested Cormorants from an oxbow lake in Arkansas, USA. Waterbirds 27, 170–176.Google Scholar
Flowers, J.R., Poore, M.F., Mullen, J.E. & Levy, M.G. (2004) Digeneans collected from piscivorous birds in North Carolina, U.S.A. Comparative Parasitology 71, 243–244.Google Scholar
Forrester, D.J. & Spalding, M.G. (2003) Parasites and diseases of wild birds in Florida. Gainsville, University Press of Florida.Google Scholar
Garcia-Varela, M., Aznar, F.J., Rodriguez, R.P. & Perez-Ponce de Leon, G. (2012) Genetic and morphological characterization of Southwellina hispida Van Cleave, 1925 (Acanthocephala: Polymorphidae), a parasite of fish eating birds. Comparative Parasitology 79, 192–201.CrossRefGoogle Scholar
Gardner, W., Mulvey, E.P. & Shaw, E.C. (1995) Regression analysis of counts and rates: poisson, overdispersed poisson, and negative binomial. Quantitative Methods in Psychology 118, 392–404.Google ScholarPubMed
Gibson, D.I., Jones, A. & Bray, R.A (2002) Keys to the Trematoda. Vol. 1. Wallingford, UK, CABI Publishing and the Natural History Museum.Google Scholar
Gibson, D.I., Bray, R.A. & Jones, A. (2005) Keys to the Trematoda. Vol. 2. Wallingford, UK, CABI Publishing and the Natural History Museum.Google Scholar
Gibson, D.I., Bray, R.A. & Jones, A. (2008) Keys to the Trematoda. Vol. 3. Wallingford, UK, CABI Publishing and the Natural History Museum.Google Scholar
Gido, K.B. & Matthews, W.J. (2000) Dynamics of the offshore fish assemblage in a southwestern reservoir (Lake Texoma, Oklahoma-Texas). Copeia 2000, 917–930.CrossRefGoogle Scholar
Gower, W.C. (1939) A modified stain and procedure for trematodes. Biotechnic and Histochemistry 14, 31–32.Google Scholar
Griffin, M.J., Khoo, L.H., Steadman, J.M., Ware, C., Quinou, S.M., Mischke, C.C., Greenway, T.E. & Wise, D.J. (2014) Chronic pathology and longevity of Drepanocephalus spathans infections in juvenile Channel Catfish. Journal of Aquatic Animal Health 26, 210–218.Google Scholar
Hanski, I. (1982) Dynamics of regional distribution: the fore and satellite species hypothesis. Oikos 38, 210–221.Google Scholar
Holl, F.J. (1932) The ecology of certain fishes and amphibians with special reference to their helminth linguatulid parasites. Ecological Monographs 2, 83–107.Google Scholar
Hutton, R.F. (1964) A second list of parasites from marine and coastal animals of Florida. Transactions of the American Microscopical Society 83, 439–447.Google Scholar
Hutton, R.F. & Sogandares-Bernal, F. (1960) Studies on helminth parasites from the coast of Florida. II. Digenic trematodes from shore birds of the west coast of Florida. Bulletin of Marine Science of the Gulf and Caribbean 10, 40–54.Google Scholar
Jackson, J.A. & Jackson, B.J.S. (1995) The Double-crested Cormorant in the south-central United States: habitat and population changes of a feathered pariah. Colonial Waterbirds 18, 118–130.CrossRefGoogle Scholar
Johnson, P.T.J. & Buller, I.D. (2011) Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions. Ecology 92, 535–541.Google Scholar
Jost, L. (2006) Entropy and diversity. Oikos 113, 363–375.Google Scholar
King, D.T. (1996) Movements of Double-crested Cormorants among winter roosts in the delta region of Mississippi. Journal of Field Ornithology 67, 205–211.Google Scholar
King, D.T., Strickland, B.K. & Radomski, A.A. (2012) Winter and summer home ranges and core use areas of Double-crested Cormorants captured near aquaculture facilities in the southeastern United States. Waterbirds 35, 124–131.Google Scholar
Kirsch, E.M. (1995) Double-crested Cormorants along the upper Mississippi River. Colonial Waterbirds 18, 131–136.Google Scholar
Krueger, R.F. (1954) A survey of the helminth parasites of fishes from Van Buren Lake and Rocky Ford Creek. Ohio Journal of Science 54, 277–297.Google Scholar
Kudlai, O., Kostadinova, A., Pulis, E.E. & Tkach, V.V. (2015) A new species of Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae) from the Double-crested Cormorant Phalacrocorax auritus (Lesson) (Aves: Phalacrocoracidae) in North America. Systematic Parasitology 90, 221–230.Google Scholar
Kuiken, T., Leighton, F.A., Wobeser, G. & Wagner, B. (1999) Causes of morbidity and mortality and their effect on reproductive success in Double-crested Cormorants from Saskatchewan. Journal of Wildlife Disease 35, 331–346.CrossRefGoogle ScholarPubMed
Leinster, T. & Cobbold, C.A. (2012) Measuring diversity: the importance of species similarity. Ecology 93, 477–489.CrossRefGoogle ScholarPubMed
Lello, J., Boag, B., Fenton, A., Stevenson, I.R. & Hudson, P.J. (2004) Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840–844.Google Scholar
McDonald, M.E. (1988) Key to Acanthocephala reported in waterfowl. Washington, DC, US Department of the Interior, Fish and Wildlife Service.Google Scholar
O'Hear, M., Pote, L., Yost, M., Doffitt, C., King, T. & Panuska, C. (2014) Morphologic and molecular identifications of digenetic trematodes in Double-crested Cormorants (Phalacrocorax auritus) from the Mississippi Delta, USA. Journal of Wildlife Disease 50, 42–49.Google Scholar
Overstreet, R.M. & Curran, S.S. (2004) Defeating diplostomoid dangers in USA catfish aquaculture. Folia Parasitologica 51, 153–165.Google Scholar
Poulin, R. & Dick, T.A. (2007) Spatial variation in population density across the geographical range in helminth parasites of yellow perch Perca flavescens . Ecography 30, 629–636.Google Scholar
Rae, M.A. (2003) Practical avian necropsy. Seminars in Avian and Exotic Pet Medicine 12, 62–70.Google Scholar
Reeder, W.G. (1951) Stomach analysis of a group of shorebirds. The Condor 53, 43–45.Google Scholar
Robinson, S.A., Forbes, M.R., Hebert, C.E. & McLaughlin, J.D. (2008) Male-biased parasitism by common helminthes is not explained by differences in body size or spleen mass of breeding cormorants Phalacrocorax auritus . Journal of Avian Biology 39, 272–276.Google Scholar
Robinson, S.A., Forbes, M.R. & Hebert, C.E. (2009) Parasitism, mercury contamination, and stable isotopes ion fish-eating Double-crested Cormorants: no support for the co-ingestion hypothesis. Canadian Journal of Zoology 87, 740–747.Google Scholar
Robinson, S.A., Forbes, M.R., Hebert, C.E. & McLaughlin, J.D. (2010) Male biased parasitism in cormorants and relationships with foraging ecology on Lake Erie, Canada. Waterbirds 33, 307–313.Google Scholar
Sheehan, K.L., Tonkyn, D.W., Yarrow, G.K. & Johnson, R.J. (2016) Parasite assemblages of Double-crested Cormorants as indicators of host populations and migration behavior. Ecological Indicators 67, 497–503.Google Scholar
Skriabin, K.I. (1964) Keys to the Trematodes of animals and man. Urbana, Illinois, University of Illinois Press.Google Scholar
Spellerberg, I.F & Fedor, P.J. (2003) A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon–Wiener’ index. Global Ecology and Biogeography 12, 177–179.Google Scholar
Sures, B. & Streit, B. (2001) Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123, 185–191.Google Scholar
Thieltges, D.W. & Poulin, R. (2016) Food-web-based comparison of the drivers of helminth parasite species richness in coastal fish and bird definitive hosts. Marine Ecology Progress Series 545, 9–19.Google Scholar
Thomas, L.J. (1937) On the life cycle of Contracaecum spiculigerum (Rud.). Journal of Parasitology 23, 429–431.Google Scholar
Threlfall, W. (1982) Endoparasites of the Double-crested Cormorant (Phalacrocorax auritus) in Florida. Proceedings of the Helminthological Society of Washington 49, 103–108.Google Scholar
Violante-Gonzalez, J., Monks, S., Gil-Guerrero, S., Rojas-Herrera, A., Flores-Garza, R. & Larumbe-Moran, E. (2011) Parasitic communities of the Neotropical Cormorant Phalacrocorax brasilianus (Gmelin) (Aves, Phalacrocoracidae) from two coastal lagoons in Guerrero state, Mexico. Parasitology Research 109, 1303–1309.Google Scholar
Wagner, B.A., Hoberg, E.P., Somers, C.M., Soos, C., Fenton, H. & Jenkins, E.J. (2012) Gastrointestinal helminth parasites of Double-crested Cormorants (Phalacrocorax auritus) at four sites in Saskatchewan, Canada. Comparative Parasitology 79, 275–282.Google Scholar
Whittaker, R.H. (1972) Evolution and measurement of species diversity. Taxon 21, 213–251.Google Scholar
Wires, L.R. & Cuthbert, F.J. (2006) Historic populations of the Double-crested Cormorant (Phalacrocorax auritus): implications for conservation and management in the 21st century. Waterbirds 29, 9–37.Google Scholar
Yamaguti, S. (1958) Systema Helminthum. New York, Interscience Publishers.Google Scholar