Parasitism, mercury contamination, and stable isotopes in fish-eating double-crested cormorants : No support for the co-ingestion hypothesis

Canadian Journal of Zoology

Volumn 87, Issue 8, 2009, Pages 740-747

  Robinson, S A ^a   Forbes, M R ^a   Hebert, C E ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FORAGING BEHAVIOR; HYPOTHESIS TESTING; MERCURY (ELEMENT); PARASITISM; SEABIRD; SEX-RELATED DIFFERENCE; STABLE ISOTOPE; STOMACH CONTENT; TROPHIC LEVEL;

AVES; CONTRACAECUM; PHALACROCORACIDAE; PHALACROCORAX AURITUS;

EID: 68949137508     PISSN: 00084301     EISSN: None     Source Type: Journal    
DOI: 10.1139/Z09-062     Document Type: Article

References (56)

1. Ackerman, J.T., Eagles-Smith, C.A., Takekawa, J.Y., Demers, S.A., Adelsbach, T.L., Bluso, J.D., Keith Miles, A., Warnock, N., Suchanek, T.H., and Schwarzbach, S.E. 2007. Mercury concentrations and space use of pre-breeding American avocets and black-necked stilts in San Francisco Bay. Sci. Total Environ. 384(1-3): 452-466. doi:10.1016/j.scitotenv.2007.04.027. PMID: 17590414.
2. Anderson, R. 2000. Nematode parasites of vertebrates: their development and transmission. 2nd ed. CABI Publishing, New York.
3. Barton, D.R., Johnson, R.A., Campbell, L., Petruniak, J., and Patterson, M. 2005. Effects of round gobies (Neogobius melanostomus) on dreissenid mussels and other invertebrates in Eastern Lake Erie, 2002-2004. J. Great Lakes Res. 31(Suppl. 2): 252-261.
4. Bearhop, S., Phillips, R.A., McGill, R., Cherel, Y., Dawson, D.A., and Croxall, J.P. 2006. Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar. Ecol. Prog. Ser. 311: 157-164. doi:10.3354/meps311157.
5. Bertrand, M., Marcogliese, D.J., and Magnan, P. 2008. Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. J. Fish Biol. 72(3): 555-572. doi:10.1111/j. 1095-8649.2007.01720.x.
6. Boroŝková, Z., Šoltys, J., and Benková, M. 1995. Effect of mercury on the immune response and mean intensity of Ascaris suum infection in guinea pigs. J. Helminthol. 69(3): 187-194. doi:10.1017/S0022149X00014139. PMID:8522763.
7. Burgess, N.M., Evers, D.C., and Kaplan, J.D. 2005. Mercury and other contaminants in common loons breeding in Atlantic Canada. Ecotoxicology, 14(1-2): 241-252. doi:10.1007/s10646-004-6271-0. PMID:15931969.
8. Bush, A.O., Fernandez, J.C., Esch, G.W., and Seed, J.R. 2001. Parasitism: The diversity and ecology of animal parasites. Cambridge University Press, Cambridge.
9. Cabana, G., and Rasmussen, J.B. 1994. Modelling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature (London), 372(6503): 255-257. doi:10.1038/372255a0.
10. Camp, J.W., Blaney, L.M., and Barnes, D.K. 1999. Helminths of the round goby, Neogobius melanostomus (Perciformes: Gobiidae), from southern Lake Michigan, Indiana. J. Helminthol. Soc. Wash. 66(1): 70-72.
11. Casaux, R., Favero, M., Silva, P., and Baroni, A. 2001. Sex differences in the diving depths and diet of Antarctic shags at the south Shetland Islands. J. Field Ornithol. 72(1): 22-29.
12. Cristol, D.A., Baker, M.B., and Carbone, C. 1999. Differential migration revisited: latitudinal segregation by age and sex class. Curr. Ornithol. 15: 33-88.
13. Fimreite, N. 1974. Mercury contamination of aquatic birds in northwestern Ontario. J. Wildl. Manage. 38(1): 120-131. doi:10.2307/3800207.
14. Fimreite, N., Brevik, E.M., and Torp, R. 1982. Mercury and organochlorines in eggs from a Norwegian gannet colony. Arch. Environ. Contam. Toxicol. 28(1): 58-60. doi:10.1007/BF01608413.
15. Forero, M.G., Hobson, K.A., Bortolotti, G.R., Donazar, J.A., Bertellotti, M., and Blanco, G. 2002. Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Mar. Ecol. Prog. Ser. 234: 289-299. doi:10.3354/meps234289.
16. France, R. 1995. Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnol. Oceanogr. 40(7): 1310-1313.
17. 15N relationships. Mar. Ecol. Prog. Ser. 174: 301-306. doi:10.3354/meps174301.
18. Glahn, J.F., and McCoy, R.B. 1995. Measurements of wintering double-crested cormorants and discriminant models of sex. J. Field Ornithol. 66(2): 299-304.
19. Glahn, J.F., Dixson, G.A., Littauer, G.A., and McCoy, R.B. 1995. Food habits of double-crested cormorants wintering in the delta region of Mississippi. Colon. Waterbirds, 18(1): 158-167. doi:10.2307/1521536.
20. Hatch, J.J., and Weseloh, D.V. 1999. Double-crested cormorant (Phalacrocorax auritus). In The birds of North America. No. 441. Edited by A. Poole and F. Gill. The Birds of North America Inc., Philadelphia. pp. 1-36.
21. Hobson, K.A., and Clark, R.G. 1992. Assessing avian diets using stable isotopes. 1. Turnover of C-13 in tissues. Condor, 94(1): 181-188. doi:10.2307/1368807.
22. Hobson, K.A., Piatt, J.F., and Pitocchelli, J. 1994. Using stable isotopes to determine seabird trophic relationships. J. Anim. Ecol. 63(4): 786-798. doi:10.2307/5256.
23. Hoffman, G.L. 1999. Parasites of North American freshwater fishes. Cornell University Press, New York.
24. Houserová, P., Kubán, V., Krácmar, S., and Sitko, J. 2007. Total mercury and mercury species in birds and fish in an aquatic ecosystem in the Czech Republic. Environ. Pollut. 145(1): 185-194. doi:10.1016/j.envpol.2006.03.027. PMID:16720064.
25. Hubbs, C.L., and Lager, K.F. 2007. Fishes of the Great Lakes region. Revised by G.R. Smith. The University of Michigan Press, Ann Arbor.
26. Hudson, P.J., and Dobson, A.P. 1991. The direct and indirect effects of the caecal nematode Trichostrongylus tenuis on red grouse. In Bird-parasite interactions: ecology, evolution, and behaviour. Edited by J.E. Loye and M. Zuk. Oxford University Press, New York. pp. 49-68.
27. Ishikawa, K., and Watanuki, Y. 2002. Sex and individual difference in foraging behavior of Japanese cormorants in years of different prey availability. J. Ethol. 20(1): 49-54. doi:10.1007/s10164-002-0053-z.
28. Johnson, J.H., Ross, R.M., McKenna, J.E., and Lewis, G.E. 2006. Estimating the size of fish consumed by double-crested cormorants: considerations for better understanding cormorant-fish interactions. J. Great Lakes Res. 32(1): 91-101. doi:10.3394/0380-1330(2006)32[91:ETSOFC]2.0. CO;2.
29. Kelly, J.F. 1999. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can. J. Zool. 78(1): 1-27. doi:10.1139/cjz-78-1-1.
30. Klein, S.L. 2000. The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24(6): 627-638. doi:10.1016/S0149-7634(00)00027-0. PMID:10940438.
31. Knudsen, R., Klemetsen, A., and Staldvik, F. 1996. Parasites as indicators of individual feeding specialisation in Arctic charr during winter in northern Norway. J. Fish Biol. 48(6): 1256-1265. doi:10.1111/j.1095- 8649.1996.tb01819.x.
32. 15N values in seabird muscle, liver and feathers. Waterbirds, 31(2): 169-178. doi:10.1675/1524-4695(2008)31[169:EOLEOC]2.0.CO;2.
33. Kvach, Y., and Stepien, C.A. 2008. Metazoan parasites of introduced round and tubenose gobies in the Great Lakes: support for the "Enemy Release Hypothesis". J. Great Lakes Res. 34(1): 23-35. doi:10.3394/0380- 1330(2008)34[23:MPOIRA]2.0.CO;2.
34. Luebke, R.W., Copeland, C.B., Diliberto, J.J., Akubue, P.I., Andrews, D.L., Riddle, M.M., Williams, W.C., and Birnbaum, L.S. 1994. Assessment of host resistance to Trichinella spiralis in mice following preinfection exposure to 2,3,7,8-TCDD. Toxicol. Appl. Pharmacol. 125(1): 7-16. doi:10.1006/taap.1994.1043. PMID:8128497.
35. Mackiewicz, J.S. 1988. Cestode transmission patterns. J. Parasitol. 74(1): 60-71. doi:10.2307/3282479. PMID:3282055.
36. Mallory, M.L., McLaughlin, J.D., and Forbes, M.R. 2007. Breeding status, contaminant burden and helminth parasites of northern fulmars Fulmarus glacialis from the Canadian high arctic. Ibis, 149(2): 338-344. doi:10.1111/j.1474-919X.2006.00636.x.
37. Marcogliese, D.J. 2002. Food webs and the transmission of parasites to marine fish. Parasitology, 124(Suppl. 7): S83-S99. doi:10.1017/ S003118200200149X. PMID:12396218.
38. McConnaughey, T., and McRoy, C.P. 1979. Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar. Biol. (N.Y.), 53(3): 257-262. doi:10.1007/BF00952434.
39. Monteiro, L.R., and Furness, R.W. 2001. Kinetics, dose-response, and excretion of methylmercury in free-living adult Cory's shearwaters. Environ. Sci. Technol. 35(4): 739-746. doi:10.1021/es000114a. PMID:11349286.
40. Newton, I. 1998. Population limitation in birds. Academic Press, London.
41. Nisbet, I.C.T., Montoya, J.P., Burger, J., and Hatch, J.J. 2002. Use of stable isotopes to investigate individual differences in diets and mercury exposures among common terns Sterna hirundo in breeding and wintering grounds. Mar. Ecol. Prog. Ser. 242: 267-274. doi:10.3354/meps242267.
42. Ricca, M.A., Keith Miles, A., and Anthony, R.G. 2008. Sources of organochlorine contaminants and mercury in seabirds from the Aleutian archipelago of Alaska: inferences from spatial and trophic variation. Sci. Total Environ. 406(1-2): 308-323. doi:10.1016/j.scitotenv.2008.06.030. PMID:18692865.
43. Robinson, S.A., Forbes, M.R., Hebert, C.E., and McLaughlin, J.D. 2008. Male-biased parasitism by common helminths is not explained by sex differences in body size or spleen mass of breeding cormorants Phalacrocorax auritus. J. Avian Biol. 39(3): 272-276. doi:10.1111/j.0908-8857.2008.04340.x.
44. Ryman, J.E., Van Walleghem, J.L.A., and Blanchfield, P.J. 2008. Methylmercury levels in a parasite (Apophallus brevis metacercariae) and its host, yellow perch (Perca flavescens). Aquat. Ecol. 42(3): 495-501. doi:10.1007/s10452-007-9104-4.
45. Sagerup, K., Henriksen, E.O., Skorping, A., Skaare, J.U., and Gabrielsen, G.W. 2000. Intensity of parasitic nematodes increases with organochlorine levels in glaucous gull. J. Appl. Ecol. 37(3): 532-539. doi:10.1046/j.1365-2664.2000.00521.x.
46. Sagerup, K., Savinov, V., Savinova, T., Kuklin, V., Muir, D.C.G., and Gabrielsen, G.W. 2009. Persistent organic pollutants, heavy metals and parasites in the glaucous gull (Larus hyperboreus) on Spitsbergen. Environ. Pollut. 157(8-9): 2282-2290. doi:10.1016/j.envpol.2009.03.031. PMID:19364623.
47. SAS Institute Inc. 1989-2000. JMP. Version 4 [computer program]. SAS Institute Inc., Cary, N.C.
48. Scott, W.B., and Crossman, E.J. 1998. Freshwater fishes of Canada. Galt House Publications Ltd., Oakville, Ont.
49. Somers, C.M., Lozer, M.N., Kjoss, V.A., and Quinn, J.S. 2003. The invasive round goby (Neogobius melanostomus) in the diet of nestling double-crested cormorants (Phalacrocorax auritus) in Hamilton Harbour, Lake Ontario. J. Great Lakes Res. 29(3): 392-399.
50. Thomas, J.D. 2002. The ecology of fish parasites with particular reference to helminth parasites and their salmonid fish hosts in Welsh rivers: a review of some of the central questions. Adv. Parasitol. 52: 1-154. doi:10.1016/S0065-308X(02)52011-X.PMID:12521260.
51. Thompson, E., Makarewicz, J.C., and Lewis, T.W. 2005. Additional link in the food web does not biomagnify a persistent contaminant in Lake Ontario: the case of Cercopagis pengoi. J. Great Lakes Res. 31(2): 210-218.
52. Wayland, M., Gilchrist, H.G., Dickson, D.L., Bollinger, T., James, C., Carreno, R.A., and Keating, J. 2001. Trace elements in king eiders and common eiders in the Canadian arctic. Arch. Environ. Contam. Toxicol. 41(4): 491-500. doi:10.1007/s002440010276.PMID:11598787.
53. Weiner, J.G., Krabbenhoft, D.P., Heinz, G.H., and Scheuhammer, A.M. 2003. Ecotoxicology of mercury. In Handbook of ecotoxicology. 2nd ed. Edited by D.J. Hoffman, B.A. Rattner, G.A. Burton, Jr., and J. Cairns, Jr. CRC Press, Boca Raton, Fla. pp. 409-463.
54. Williamson, C.E. 1991. Copepoda. In Ecology and classification of North American freshwater invertebrates. Edited by J.H. Thorp and A.P. Covich. Academic Press, New York. pp. 787-813.
55. Withers, K., and Brooks, T.S. 2004. Diet of double-crested cormorants (Phalacrocorax auritus) wintering on the central Texas coast. Southwest. Nat. 49(1): 48-53. doi:10.1894/0038-4909(2004)049<0048:DODCPA>2.0. CO;2.
56. Zar, J.H. 1996. Biostatistical analysis. Prentice-Hall, Inc., Upper Saddle River, N.J.