Contamination of mercury during the wintering period influences concentrations at breeding sites in two migratory piscivorous birds

Environmental Science and Technology

Volumn 48, Issue 23, 2014, Pages 13694-13702

  Lavoie, Raphael A ^a   Baird, Christopher J ^a   King, Laura E ^b   Kyser, T Kurt ^a   Friesen, Vicki L ^a   Campbell, Linda M ^a,c  

^a QUEEN S UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c SAINT MARY S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FISH; ISOTOPES; LAKES; MERCURY (METAL);

EXPOSURE GROUPS; HG CONCENTRATIONS; ISOTOPIC SIGNATURES; MERCURY CONCENTRATIONS; MIGRATORY FISHES; PHALACROCORAX AURITUS; PISCIVOROUS BIRDS; TEMPORAL TRENDS;

BIRDS;

MERCURY; STABLE ISOTOPE;

BIOMONITORING; BIRD; BREEDING SITE; CONCENTRATION (COMPOSITION); MERCURY (ELEMENT); MIGRATORY POPULATION; POLLUTION MONITORING; STABLE ISOTOPE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRD; BREEDING; CIRCANNUAL RHYTHM; FEEDING ECOLOGY; FEMALE; FOOD WEB; MALE; MIGRATORY SPECIES; NONHUMAN; OVERWINTERING; QUALITY CONTROL; SEA POLLUTION; SEASONAL VARIATION; SUMMER; TURNOVER TIME; WATER CONTAMINATION; WINTER; ANIMAL; ANIMAL FOOD; BLOOD; CANADA; CHEMISTRY; ECOSYSTEM; FEATHER; FISH; PHYSIOLOGY; POLLUTION; POPULATION MIGRATION; SEASON;

GREAT LAKES [NORTH AMERICA]; LAKE ONTARIO;

AVES; HYDROPROGNE CASPIA; PHALACROCORAX AURITUS; STERNA CASPIA;

ANIMAL MIGRATION; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BIRDS; BREEDING; ECOSYSTEM; ENVIRONMENTAL POLLUTION; FEATHERS; FEMALE; FISHES; MALE; MERCURY; ONTARIO; SEASONS;

EID: 84918837803     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es502746z     Document Type: Article

References (50)

1. Elliott, J. E.; Elliott, K. H. Tracking marine pollution Science 2013, 340, 556-558
2. Borgå, K.; Kidd, K. A.; Muir, D. C. G.; Berglund, O.; Conder, J. M.; Gobas, F. A. P. C.; Kucklick, J.; Malm, O.; Powell, D. E. Trophic magnification factors: considerations of ecology, ecosystems, and study design Integr. Environ. Assess. Manage. 2012, 8, 64-84
3. Fort, J.; Robertson, G. J.; Grémillet, D.; Traisnel, G.; Bustamante, P. Spatial ecotoxicology: migratory Arctic seabirds are exposed to mercury contamination while overwintering in the northwest Atlantic Environ. Sci. Technol. 2014, 48, 11560-11567
4. Lavoie, R. A.; Kyser, T. K.; Campbell, L. M. Migration patterns affect biomagnifying contaminant concentrations in fish-eating birds Integr. Environ. Assess. Manage. 2012, 8, 200-202
5. Cabana, G.; Rasmussen, J. B. Modeling food-chain structure and contaminant bioaccumulation using stable nitrogen isotopes Nature 1994, 372, 255-257
6. Cabana, G.; Rasmussen, J. B. Comparison of aquatic food chains using nitrogen isotopes Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 10844-10847
7. Fry, B.; Sherr, E. B. Delta-C-13 measurements as indicators of carbon flow in marine and fresh-water ecosystems Contrib. Mar. Sci. 1984, 27, 13-47
8. 15N incorporation in house sparrows (Passer domesticus) Oecologia 2005, 144, 226-232
9. Gonzalez-Solis, J.; Smyrli, M.; Militao, T.; Gremillet, D.; Tveraa, T.; Phillips, R. A.; Boulinier, T. Combining stable isotope analyses and geolocation to reveal kittiwake migration Mar. Ecol.: Prog. Ser. 2011, 435, 251-274
10. UNEP The global atmospheric mercury assessment: sources, emissions and transport; United Nations Environment Programme, Chemicals Branch: Geneva, Switzerland, 2008; 42p.
11. Scheuhammer, A. M.; Meyer, M. W.; Sandheinrich, M. B.; Murray, M. W. Effects of environmental methylmercury on the health of wild birds, mammals, and fish Ambio 2007, 36, 12-18
12. Lavoie, R. A.; Jardine, T. D.; Chumchal, M. M.; Kidd, K. A.; Campbell, L. Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis Environ. Sci. Technol. 2013, 47, 13385-13394
13. Lavoie, R. A.; Hebert, C. E.; Rail, J. F.; Braune, B.; Yumvihoze, E.; Hill, L. G.; Lean, D. R. S. Trophic structure and mercury distribution in a Gulf of St. Lawrence (Canada) food web using stable isotope analysis Sci. Total Environ. 2010, 408, 5529-5539
14. Bond, A. L.; Diamond, A. W. Total and methyl mercury concentrations in seabird feathers and eggs Arch. Environ. Contam. Toxicol. 2009, 56, 286-291
15. Kim, E. Y.; Murakami, T.; Saeki, K.; Tatsukawa, R. Mercury levels and its chemical form in tissues and organs of seabirds Arch. Environ. Contam. Toxicol. 1996, 30, 259-266
16. Evers, D. C.; Burgess, N. M.; Champoux, L.; Hoskins, B.; Major, A.; Goodale, W. M.; Taylor, R. J.; Poppenga, R.; Daigle, T. Patterns and interpretation of mercury exposure in freshwater avian communities in Northeastern North America Ecotoxicology 2005, 14, 193-221
17. Evers, D. C.; Han, Y. J.; Driscoll, C. T.; Kamman, N. C.; Goodale, M. W.; Lambert, K. F.; Holsen, T. M.; Chen, C. Y.; Clair, T. A.; Butler, T. Biological mercury hotspots in the northeastern United States and southeastern Canada Bioscience 2007, 57, 29-43
18. Hatch, J. J.; Weseloh, D. V. Double-crested Cormorant (Phalacrocorax auritus) In The Birds of North America Online; Poole, A.; Gill, F., Eds.; Cornell Lab of Ornithology: New York, USA, 1999. URL: http://bna.birds.cornell.edu/bna/species/441 (accessed April 15, 2014).
19. Cuthbert, F. J.; Wires, L. R. Caspian Tern (Sterna caspia) In The Birds of North America Online; Poole, A.; Gill, F., Eds.; Cornell Lab of Ornithology: New York, USA, 1999. URL: http://bna.birds.cornell.edu/bna/species/403 (accessed April 15, 2014).
20. Szep, T.; Hobson, K. A.; Vallner, J.; Piper, S. E.; Kovacs, B.; Szabo, D. Z.; Møller, A. P. Comparison of trace element and stable isotope approaches to the study of migratory connectivity: an example using two hirundine species breeding in Europe and wintering in Africa J. Ornithol. 2009, 150, 621-636
21. Bearhop, S.; Ruxton, G. D.; Furness, R. W. Dynamics of mercury in blood and feathers of great skuas Environ. Toxicol. Chem. 2000, 19, 1638-1643
22. Burger, J.; Nisbet, I. C. T.; Gochfeld, M. Metal levels in regrown feathers: assessment of contamination on the wintering and breeding grounds in the same individuals J. Toxicol. Environ. Health 1992, 37, 363-374
23. Burger, J.; Gochfeld, M. Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean Sci. Total Environ. 2000, 257, 37-52
24. Wassenaar, L. I. An introduction to light stable isotopes for use in terrestrial animal migration studies. In Tracking Animal migration with stable isotopes; Hobson, K. A.; Wassenaar, L. I., Eds.; Academic Press: Oxford, UK, 2008; 152p.
25. Gibson, L. A.; Lavoie, R. L.; Bissegger, S.; Campbell, L. M.; Langlois, V. S. A positive correlation between mercury and oxidative stress-related gene expression (GPX3 and GSTM3) is measured in female Double-crested Cormorant blood Ecotoxicology 2014, 23, 1004-1014
26. U.S. EPA Method 1631: Revision E, mercury in water by oxidation, purge and trap, and cold vapor atomic fluorescence spectrometry; U.S. Environmental Protection Agency: Washington, USA, 2002. URL: http://www.epa.gov (accessed May 13, 2010).
27. Sambrook, J.; Russell, D. W. Molecular cloning: a laboratory manual, 3 rd ed.; Cold Spring Harbor Laboratory Press: New York, 2001.
28. Fridolfsson, A. K.; Ellegren, H. A simple and universal method for molecular sexing of non-ratite birds J. Avian Biol. 1999, 30, 116-121
29. R Core Team R: A language and environment for statistical computing; R Foundation for Statistical Computing: Vienna, Austria, 2013. URL: http://www.R-project.org/ (April 13, 2014).
30. Barton, K. MuMIn: Multi-model inference; R package version 1.9.13; 2013. URL: http://CRAN.R-project.org/package=MuMIn (accessed April 13, 2014).
31. Quillfeldt, P.; Bugoni, L.; McGill, R. R.; Masello, J.; Furness, R. Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies Mar. Biol. 2008, 155, 593-598
32. Bates, D.; Maechler, M.; Bolker, B.; Walker, S. lme4: Linear mixed-effects models using Eigen and S4; R package version 1.0-5; 2013. URL: http://CRAN.R-project.org/package=lme4 (accessed April 13, 2014).
33. Robinson, S. A.; Lajeunesse, M. J.; Forbes, M. R. Sex differences in mercury contamination of birds: testing multiple hypotheses with meta-analysis Environ. Sci. Technol. 2012, 46, 7094-7101
34. Ofukany, A. F. A.; Hobson, K. A.; Wassenaar, L. I. Connecting breeding and wintering habitats of migratory piscivorous birds: implications for tracking contaminants (Hg) using multiple stable isotopes Environ. Sci. Technol. 2012, 46, 3263-3272
35. Fournier, F.; Karasov, W. H.; Kenow, K. P.; Meyer, M. W.; Hines, R. K. The oral bioavailability and toxicokinetics of methylmercury in Common Loon (Gavia Immer) chicks Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2002, 133, 703-714
36. Eagles-Smith, C. A.; Ackerman, J. T.; Yee, J.; Adelsbach, T. L. Mercury demethylation in waterbird livers: dose-response thresholds and differences among species Environ. Toxicol. Chem. 2009, 28, 568-577
37. Henny, C. J.; Hill, E. F.; Hoffman, D. J.; Spalding, M. G.; Grove, R. A. Nineteenth century mercury: Hazard to wading birds and cormorants of the Carson River, Nevada Ecotoxicology 2002, 11, 213-231
38. Braune, B. M.; Gaskin, D. E. Mercury levels in Bonapartes Gulls (Larus philadelphia) during autumn molt in the Quoddy Region, New-Brunswick, Canada Arch. Environ. Contam. Toxicol. 1987, 16, 539-549
39. Agusa, T.; Matsumoto, T.; Ikemoto, T.; Anan, Y.; Kubota, R.; Yasunaga, G.; Kunito, T.; Tanabe, S.; Ogi, H.; Shibata, Y. Body distribution of trace elements in black-tailed gulls from Rishiri Island, Japan: Age-dependent accumulation and transfer to feathers and eggs Environ. Toxicol. Chem. 2005, 24, 2107-2120
40. Honda, K.; Nasu, T.; Tatsukawa, R. Seasonal-changes in mercury accumulation in the Black-eared Kite, Milvus migrans Lineatus Environ. Pollut. 1986, 42, 325-334
41. Braune, B. M.; Gaskin, D. E. A mercury budget for the Bonapartes Gull during autumn molt Ornis Scand. 1987, 18, 244-250
42. Monteiro, L. R.; Furness, R. W. Kinetics, dose-response, and excretion of methylmercury in free-living adult Cory's shearwaters Environ. Sci. Technol. 2001, 35, 739-746
43. Pyle, P. Identification guide to North American birds. Part II; Slate Creek Press: Point Reyes Station, USA, 2008; 835p.
44. French, T. D.; Campbell, L. M.; Jackson, D. A.; Casselman, J. M.; Scheider, W. A.; Hayton, A. Long-term changes in legacy trace organic contaminants and mercury in Lake Ontario salmon in relation to source controls, trophodynamics, and climatic variability Limnol. Oceanogr. 2006, 51, 2794-2807
45. Weseloh, D. V. C.; Moore, D. J.; Hebert, C. E.; de Solla, S. R.; Braune, B. M.; McGoldrick, D. J. Current concentrations and spatial and temporal trends in mercury in Great Lakes Herring Gull eggs, 1974-2009 Ecotoxicology 2011, 20, 1644-1658
46. Belant, J. L.; Tyson, L. A.; Mastrangelo, P. A. Effects of lethal control at aquaculture facilities on populations of piscivorous birds Wildl. Soc. Bull. 2000, 28, 379-384
47. Baird, C. J. Mercury and stable isotopes in Common Terns (Sterna hirundo) from the St. Lawrence River: a comparison between breeding and winter habitats. M.Sc. Thesis, Queen's University, Kingston, Canada, 2013.
48. Cherel, Y.; Le Corre, M.; Jaquemet, S.; Menard, F.; Richard, P.; Weimerskirch, H. Resource partitioning within a tropical seabird community: new information from stable isotopes Mar. Ecol.: Prog. Ser. 2008, 366, 281-291
49. Labbé, A. M. T.; Dunlop, J. N.; Loneragan, N. R. Central place foraging and feather regrowth rate in bridled terns (Onychoprion anaethetus): an insight from stable isotopes Mar. Freshwater Res. 2013, 64, 1184-1191
50. Dorr, B. S.; Taylor, J. D.; Werner, S. J.; King, D. T.; Farquhar, J. F.; Mazzocchi, I. M.; McCullough, R. D. Summer and migrational movements of satellite-marked Double-crested Cormorants from a breeding colony managed by egg-oiling in Lake Ontario, USA Waterbirds 2012, 35, 114-123