Thyroid Hormones, Retinol and Clinical Parameters in Relation to Mercury and Organohalogen Contaminants in Great Blue Heron (Ardea herodias) Nestlings from the St. Lawrence River, Québec, Canada

Article

Abstract

The exposure and effects of persistent environmental contaminants were investigated in great blue heron (Ardea herodias) nestlings sampled in 2001, 2002, 2006, and 2007 in freshwater and estuarine heronries along the St. Lawrence River, Québec (Canada). Biomarkers (retinoids, thyroid hormones, and clinical parameters) and contaminants (organochlorine contaminants, polychlorinated biphenyls (PCBs), brominated flame retardants (BFRs), and mercury (Hg)) were analyzed in blood, and Hg was analyzed in feathers (generally 9 nestlings per colony and 4 colonies per year). Feather Hg and most contaminants detected in blood were found in higher concentrations in birds from freshwater than estuarine colonies more distant from the pollution sources. Among freshwater colonies, Ile aux Hérons showed the highest levels of contaminants, with mean Hg concentrations of 8.4 and 0.55 mg/kg in feathers and plasma, respectively, and plasma ΣBFRs of 19.6 ng/g ww. The highest mean ΣPCBs, 56.5 ng/g ww, was measured at Grande Ile in 2001. The levels of contaminants in heron nestlings were generally below critical thresholds for adverse effects observed on reproduction or survival. Retinol, dehydroretinol (DROH), and thyroid hormone concentrations differed significantly among colonies. Retinol concentrations were negatively related to ΣPCBs, whereas DROH concentrations were negatively related to Hg and total and free triiodothyronine (T3) concentrations were negatively related to ΣBFRs. These results indicate that contaminants from the St. Lawrence River could impair the development and fitness of great blue heron nestlings and emphasize the need for more research on the great blue heron population to assess their health and nutritional status.

Supplementary material

244_2017_364_MOESM1_ESM.docx (65 kb)
Supplementary material 1 (DOCX 64.8 kb)
244_2017_364_MOESM2_ESM.docx (26 kb)
Supplementary material 2 (DOCX 25.5 kb)
244_2017_364_MOESM3_ESM.docx (20 kb)
Supplementary material 3 (DOCX 19 kb)

References

  1. Abdennadher A, Ramírez F, Romdhane MS, Ruiz X, Jover L, Sanpera C (2011) Little egret (Egretta garzetta) as a bioindicator of trace element pollution in Tunisian aquatic ecosystems. Environ Monit Assess 175:677–684CrossRefGoogle Scholar
  2. Becker PH, Henning D, Furness RW (1994) Differences in mercury contamination and elimination during feather development in gull and tern broods. Arch Environ Contam Toxicol 27:162–167CrossRefGoogle Scholar
  3. Benoit JM, Mason RP, Gilmour CC (1999) Estimation of mercury-sulfide speciation in sediment pore waters using octanol-water partitioning and implications for availability to methylating bacteria. Environ Toxicol Chem 18:2138–2141Google Scholar
  4. Bishop CA, Mahony NA, Trudeau S, Pettit KE (1999) Reproductive success and biochemical effects in tree swallows (Tachycineta bicolor) exposed to chlorinated hydrocarbon contaminants in wetlands of the Great Lakes and St. Lawrence River Basin, USA and Canada. Environ Toxicol Chem 18:263–271CrossRefGoogle Scholar
  5. Boily M, Champoux L, Bourbonnais D, DesGranges JL, Rodrigue J, Spear P (1994) ß-carotene and retinoids in eggs of great blue herons (Ardea herodias) in relation to St. Lawrence contamination. Ecotoxicology 3:271–286CrossRefGoogle Scholar
  6. Boily M, Ndayibagira A, Spear P (2003a) Influence of mono-ortho PCBs on retinoid hydrolase and esterification activities in the yolk sac membrane of Japanese quail eggs. Comp Biochem Phys C 134:11–23Google Scholar
  7. Boily M, Ndayibagira A, Spear P (2003b) Retinoids, LRAT and REH activities in eggs of Japanese quail following maternal and in ovo exposures to 3,3′,4,4′-tetrachlorobiphenyl. Ecotoxicology 12:9–21CrossRefGoogle Scholar
  8. Braune BM, Trudeau S, Jeffrey DA, Mallory ML (2011) Biomarker responses associated with halogenated organic contaminants in northern fulmars (Fulmarus glacialis) breeding in the Canadian Arctic. Environ Pollut 159:2891–2898CrossRefGoogle Scholar
  9. Brouwer AD, Morse C, Lans MC, Schuur AG, Murk AJ, Klasson-Wehler E, Bergman Å, Visser TJ (1998) Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol Ind Health 14:59–84CrossRefGoogle Scholar
  10. Bryan AL Jr, Brant HA, Jagoe CH, Romanek CS, Brisbin IL Jr (2012) Mercury concentrations in nestling wading birds relative to diet in the Southeastern United States: a stable isotope analysis. Arch Environ Contam Toxicol 63:144–152CrossRefGoogle Scholar
  11. Bustnes JO, Erikstad KE, Lorentsen SH, Herzke D (2008) Perfluorinated and chlorinated pollutants as predictors of demographic parameters in an endangered seabird. Environ Pollut 156:417–424CrossRefGoogle Scholar
  12. Cadieux MA, Muir DCG, Béland P, Hickie BE (2016) Lactational transfer of polychlorinated-biphenyls (PCBs) and other organochlorines in St. Lawrence beluga whales (Delphinapterus leucas). Arch Environ Contam Toxicol 70:169–179CrossRefGoogle Scholar
  13. Cesh LS, Elliott KH, Quade S, Mckinney MA, Maisoneuve F, Garcelon DK, Sandau CD, Letcher RJ, Williams TD, Elliott JE (2010) Polyhalogenated aromatic hydrocarbons and metabolites: relation to circulating thyroid hormone and retinol in nestling bald eagles (Haliaeetus leucocephalus). Environ Toxicol Chem 29:1301–1310CrossRefGoogle Scholar
  14. Champoux L, Rodrigue J, DesGranges JL, Trudeau S, Hontela A, Boily M, Spear PA (2002) Assessment of contamination and biomarker responses in two species of Herons on the St. Lawrence River. Environ Monit Assess 79:193–215CrossRefGoogle Scholar
  15. Champoux L, Rodrigue J, Trudeau S, Boily M, Spear PA, Hontela A (2006) Contamination and biomarkers in the great blue heron, an indicator of the state of the St. Lawrence River. Ecotoxicology 15:83–96CrossRefGoogle Scholar
  16. Champoux L, Moisey J, Muir DCG (2010) Polybrominated diphenylethers, toxaphenes, and other halogenated organic pollutants in great blue heron eggs. Environ Toxicol Chem 29:243–249CrossRefGoogle Scholar
  17. Chen D, Letcher RJ, Burgess NM, Champoux L, Elliott JE, Hebert CE, Martin P, Wayland M, Weseloh DVC, Wilson L (2012) Flame retardants in eggs of four gull species (Laridae) from breeding sites spanning Atlantic to Pacific Canada. Environ Pollut 168:1–9CrossRefGoogle Scholar
  18. Cole A, Steffen A, Eckley C, Narayan J, Pilote M, Tordon R, Graydon J, St. Louis V, Xu X, Branfireun B (2014) A survey of mercury in air and precipitation across Canada: patterns and trends. Atmosphere 5:635–668CrossRefGoogle Scholar
  19. Custer CM, Read LB (2006) Polychlorinated biphenyl congener patterns in tree swallows (Tachycineta bicolor) nesting in the Housatonic River watershed, western Massachusetts, USA, using a novel statistical approach. Environ Pollut 142:235–245CrossRefGoogle Scholar
  20. Darnerud PO (2003) Toxic effects of brominated flame retardants in man and in wildlife. Environ Int 29:841–853CrossRefGoogle Scholar
  21. Defo MA, Spear PA, Couture P (2014) Consequences of metal exposure on retinoid metabolism in vertebrates: a review. Toxicol Lett 225:1–11CrossRefGoogle Scholar
  22. DesGranges JL, Desrosiers A (2005) Breeding distribution and population trends of the great blue heron in Quebec, 1977–2001. Canadian Wildlife Service, Occasional paper no. 113Google Scholar
  23. DeWitt JC, Millsap DS, Yeager RL, Heise SS, Sparks DW, Henshel DS (2006) External heart deformities in passerine birds exposed to environmental mixtures of polychlorinated biphenyls during development. Environ Toxicol Chem 25:541–551CrossRefGoogle Scholar
  24. Doyon C, Boileau S, Fortin R, Spear PA (1998) Rapid HPLC analysis of retinoids and dehydroretinoids stored in fish liver: comparison of two lake sturgeon populations. J Fish Biol 53:973–986CrossRefGoogle Scholar
  25. Drouillard KG, Fernie KJ, Smits JE, Bortolotti GR, Bird DM, Norstrom RJ (2001) Quantifying maternal and dietary sources of 2,2,4,4,5,5-hexachlorobiphenyl deposited in eggs of the ring dove (Streptopelia risoria). Environ Toxicol Chem 20:561–567CrossRefGoogle Scholar
  26. Elliott JE, Harris ML (2001) An ecotoxicological assessment of chlorinated hydrocarbon effects on bald eagle populations. Rev Toxicol 4:1–60Google Scholar
  27. Elliott JE, Wilson LK, Henny CJ, Trudeau SF, Leighton FA, Kennedy SW, Cheng KM (2001) Assessment of biological effects of chlorinated hydrocarbons in osprey chicks. Environ Toxicol Chem 20:866–879CrossRefGoogle Scholar
  28. Environment Canada (2004) Canadian acid deposition science assessment, Environment Canada. http://epe.lac-bac.gc.ca/100/200/301/environment_can/msc-smc/2004_canadian_acid_deposition-e/En4-46-2004E.pdf. Accessed 26 Jan 2015
  29. Eulaers I, Jaspers VLB, Halley DJ, Lepoint G, Nygård T, Pinxten R, Covaci A, Eens M (2014) Brominated and phosphorus flame retardants in white-tailed eagle Haliaeetus albicilla nestlings: bioaccumulation and associations with dietary proxies (δ13C, δ15N and δ34S). Sci Tot Environ 478:48–57CrossRefGoogle Scholar
  30. Fernie KJ, Shutt JL, Mayne G, Hoffman D, Letcher RJ, Drouillard KG, Ritchie IJ (2005) Exposure to polybrominated diphenyl ethers (PBDEs): changes in thyroid, vitamin A, glutathione homeostasis, and oxidative stress in American kestrels (Falco sparverius). Toxicol Sci 88:375–383CrossRefGoogle Scholar
  31. Fournier F, Karasov WH, Kenow KP, Meyer MW, Hine RK (2002) The oral bioavailability and toxicokinetics of methylmercury in common loon (Gavia immer) chicks. Comp Biochem Phys A 133:703–714CrossRefGoogle Scholar
  32. Fox GA, Jeffrey DA, Williams KS, Kennedy SW, Grasman KA (2007) Health of herring gulls (Larus argentatus) in relation to breeding location in the early 1990s. I. Biochemical measures. J Toxicol Environ Health A 70:1443–1470CrossRefGoogle Scholar
  33. Gariboldi JC, Jagoe CH, Bryan AL Jr (1998) Dietary exposure to mercury in nestling wood storks (Mycteria americana) in Georgia. Arch Environ Contam Toxicol 34:398–405CrossRefGoogle Scholar
  34. Gariboldi JC, Bryan AL Jr, Jagoe CH (2001) Annual and regional variation in mercury concentrations in wood stork nestlings. Environ Toxicol Chem 20:1551–1556CrossRefGoogle Scholar
  35. Gee GF, Carpenter JW, Hensler GL (1981) Species differences in hematological values of captive cranes, geese, raptors and quails. J Wildl Manag 45:463–483CrossRefGoogle Scholar
  36. Gentes ML, Letcher RJ, Caron-Beaudoin E, Verreault J (2012) Novel flame retardants in urban-feeding ring-billed gulls from the St. Lawrence River, Canada. Environ Sci Technol 46:9735–9744CrossRefGoogle Scholar
  37. Gesto M, Filipe L, Castro C, Reis-Henriques MA, Santos MM (2012) Tissue-specific distribution patterns of retinoids and didehydroretinoids in rainbow trout Oncorhynchus mykiss. Comp Biochem Phys B 161:69–78CrossRefGoogle Scholar
  38. Grasman KA, Fox GA, Scanlon PF, Ludwig JP (1996) Organochlorine-associated immunosuppression in prefledgling caspian terns and herring gulls from the Great Lakes: an epidemiological study. Environ Health Perspect 104:829–842CrossRefGoogle Scholar
  39. Harris ML, Elliott JE (2011) Effects of polychlorinated biphenyls, dibenzo-p-dioxins and dibenzofurans, and polybrominated diphenyl ethers in wild birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations, 2nd edn. CRC Press, Boca Raton, pp 477–529CrossRefGoogle Scholar
  40. Harris ML, Elliott JE, Butler RW, Wilson LK (2003) Reproductive success and chlorinated hydrocarbon contamination of resident great blue herons (Ardea herodias) from Coastal British Columbia, Canada, 1977 to 2000. Environ Pollut 121:207–227CrossRefGoogle Scholar
  41. Harris ML, Wilson LK, Trudeau SF, Elliott JE (2007) Vitamin A and contaminant concentrations in surf scoters (Melanitta perspicillata) wintering on the Pacific coast of British Columbia, Canada. Sci Total Environ 378:366–375CrossRefGoogle Scholar
  42. Head JA, DeBofsky A, Hinshaw J, Basu N (2011) Retrospective analysis of mercury content in feathers of birds collected from the state of Michigan (1895–2007). Ecotoxicology 20:1636–1643CrossRefGoogle Scholar
  43. Hoffman DJ, Spalding MG, Frederick PC (2005) Subchronic effects of methylmercury on plasma and organ biochemistries in great egret nestlings. Environ Toxicol Chem 24:3078–3084CrossRefGoogle Scholar
  44. Houle D, Gagnon C, Couture S, Kemp A (2004) Recent recovery of lake water quality in southern Québec following reductions in sulfur emissions. Water Air Soil Pollut 4:247–261CrossRefGoogle Scholar
  45. Kenow KP, Grasman KA, Hines RK, Meyer MW, Gendron-Fitzpatrick A, Spalding MG, Gray BR (2007) Effects of methylmercury exposure on the immune function of juvenile common loons (Gavia immer). Environ Toxicol Chem 26:1460–1469CrossRefGoogle Scholar
  46. Kenow KP, Hoffman DJ, Hines RK, Meyer MW, Bickham JW, Matson CW, Stebbins CW, Montagna P, Abdulaziz Elfessi A (2008) Effects of methylmercury exposure on glutathione metabolism, oxidative stress, and chromosomal damage in captive-reared common loon (Gavia immer) chicks. Environ Pollut 156:732–738CrossRefGoogle Scholar
  47. Letcher RJ, Mattioli LC, Marteinson SC, Bird D, Ritchie IJ, Fernie KJ (2015) Uptake, distribution, depletion and in ovo transfer of isomers of hexabromocyclododecane flame retardant in diet-exposed American kestrels (Falco sparverius). Environ Toxicol Chem 34:1103–1112CrossRefGoogle Scholar
  48. Marteinson SC, Bird DM, Shutt JL, Letcher RJ, Ritchie IJ, Fernie KJ (2010) Multi-generational effects of polybrominated diphenylethers exposure: embryonic exposure of male American kestrels (Falco sparverius) to DE-71 alters reproductive success and behaviors. Environ Toxicol Chem 29:1740–1747Google Scholar
  49. McKinney MA, Cesh LS, Elliott JE, Williams TD, Garcelon DK, Letcher RJ (2006) Brominated flame retardants and halogenated phenolic compounds in North American west coast bald eaglet (Haliaeetus leucocephalus) plasma. Environ Sci Technol 40:6275–6281CrossRefGoogle Scholar
  50. McNabb AFM (2006) Avian thyroid development and adaptive plasticity. Gen Comp Endocr 147:93–101CrossRefGoogle Scholar
  51. Meyer MW, Evers DC, Hartigan JJ, Rasmussen PS (1998) Patterns of common loon (Gavia immer) mercury exposure, reproduction, and survival in Wisconsin, USA. Environ Toxicol Chem 17:184–190CrossRefGoogle Scholar
  52. Miller MD, Crofton KM, Rice DC, Zoeller RT (2009) Thyroid-disrupting chemicals: interpreting upstream biomarkers of adverse outcomes. Environ Health Perspect 117:1033–1041CrossRefGoogle Scholar
  53. Moise AR, Domínguez M, Alvarez S, Alvarez R, Schupp M, Cristancho AG, Kiser PD, de Lera AR, Lazar MA, Palczewski K (2008) Stereospecificity of retinol saturase: Absolute configuration, synthesis, and biological evaluation of dihydroretinoids. J Am Chem Soc 130:1154–1155CrossRefGoogle Scholar
  54. Müller K, Raila J, Altenkamp R, Schmidt D, Dietrich R, Hurtienne A, Wink M, Krone O, Brunnberg L, Schweigert FL (2012) Concentrations of retinol, 3,4-didehydroretinol, and retinyl esters in plasma of free-ranging birds of prey. J Anim Physiol Anim Nutr 96:1044–1053CrossRefGoogle Scholar
  55. Murvoll KM, Skaare JU, Anderssen E, Jenssen BM (2006) Exposure and effects of persistent organic pollutants in European shag (Phalacrocorax aristotelis) hatchlings from the coast of Norway. Environ Toxicol Chem 25:190–198CrossRefGoogle Scholar
  56. Neugebauer EA, Sans Cartier GL, Wakeford BJ (2000) Methods for the determination of metals in wildlife tissues using various atomic absorption spectrophotometry techniques. Technical Report Series no. 337E. Canadian Wildlife Service, Headquarters, Hull, Québec, CanadaGoogle Scholar
  57. Newman SH, Padula VM, Cray C, Kramer LD (2007) Health assessment of black-crowned night-herons (Nycticorax nycticorax) of the New York Harbor estuary. Comp Biochem Phys B 148:363–374CrossRefGoogle Scholar
  58. Novák J, Beníšek M, Hilscherová K (2008) Disruption of retinoid transport, metabolism and signaling by environmental pollutants. Environ Int 34:898–913CrossRefGoogle Scholar
  59. Polo FJ, Celdrhn J, Viscor G, Palomeque J (1994) Blood chemistry of captive herons, egrets, spoonbill, ibis and gallinule. Comp Biochem Physiol 107A:343–347CrossRefGoogle Scholar
  60. Power DM, Elias NP, Richardson SJ, Mendes J, Soares CM, Santos CRA (2000) Evolution of the thyroid hormone-binding protein, transthyretin. Gen Comp Endocr 119:241–255CrossRefGoogle Scholar
  61. Quinney TE (1982) Growth, diet, and mortality of nestling great blue herons. Wilson Bull 94:571–577Google Scholar
  62. Rattner BA, Hoffman DJ, Melancon MJ, Olsen GH, Schmidt SR, Parsons KC (2000) Organochlorine and metal contaminant exposure and effects in hatching black-crowned night herons (Nycticorax nycticorax) in Delaware Bay. Arch Environ Contam Toxicol 39:38–45CrossRefGoogle Scholar
  63. Rivera-Rodríguez LB, Rodríguez-Estrella R (2011) Incidence of organochlorine pesticides and the health condition of nestling ospreys (Pandion haliaetus) at Laguna San Ignacio, a pristine area of Baja California Sur, Mexico. Ecotoxicology 20:29–38CrossRefGoogle Scholar
  64. Rolland RM (2000) A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. J Wildl Dis 36:615–635CrossRefGoogle Scholar
  65. Ross SA, McCaffery PJ, Drager UC, De Luca LM (2000) Retinoids in embryonal development. Physiol Rev 80:1021–1054Google Scholar
  66. Santos CSA, Monteiro MS, Soares AMVM, Loureiro S (2012) Characterization of cholinesterases in plasma of three Portuguese native bird species: application to biomonitoring. PLoS ONE 7(3):e33975. doi:10.1371/journal.pone.0033975 CrossRefGoogle Scholar
  67. Scheuhammer AM (1991) Effects of acidification on the bioavailability of toxic metals and calcium to wild birds and mammals. Environ Pollut 71:329–375CrossRefGoogle Scholar
  68. Scheuhammer AM, Perrault JA, Bond DE (2001) Mercury, methylmercury, and selenium concentrations in eggs of common loons (Gavia immer) from Canada. Environ Monit Assess 72:79–94CrossRefGoogle Scholar
  69. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–17CrossRefGoogle Scholar
  70. Sepulveda MS, Frederick PC, Spalding MG, Williams GE (1999) Mercury contamination in free-ranging great egret nestlings (Ardea albus) from Southern Florida, USA. Environ Toxicol Chem 18:985–992CrossRefGoogle Scholar
  71. Sonne C, Bustnes JO, Herzke D, Jaspers VLB, Covaci A, Eulaers I, Halley DJ, Moum T, Ballesteros M, Eens M, Ims RA, Hanssen SA, Erikstad KE, Johnsen TV, Rigét FF, Jensen AL, Kjelgaard-Hansen M (2012) Blood plasma clinical–chemical parameters as biomarker endpoints for organohalogen contaminant exposure in Norwegian raptor nestlings. Ecotoxicol Environ Saf 80:76–83CrossRefGoogle Scholar
  72. Spear PA, Bourbonnais DH, Norstrom RJ, Moon TW (1990) Yolk retinoids (vitamin A) in eggs of the herring gull and correlations with polychlorinated dibenzo-p-dioxins and dibenzofurans. Environ Toxicol Chem 9:1053–1061CrossRefGoogle Scholar
  73. Su G, Letcher RJ, Moore JN, Williams LL, Martin PA, de Solla SR, Bowerman WW (2015) Spatial and temporal comparisons of legacy and emerging flame retardants in herring gull eggs from colonies spanning the Laurentian Great Lakes of Canada and United States. Environ Res 142:720–730CrossRefGoogle Scholar
  74. Ucán-Marín F, Arukwe A, Mortensen A, Gabrielsen GW, Fox GA, Letcher RJ (2009) Recombinant transthyretin purification and competitive binding with organohalogen compounds in two gull species (Larus argentatus and Larus hyperboreus). Toxicol Sci 107:440–450CrossRefGoogle Scholar
  75. Venier M, Wierda M, Bowerman WW, Hites RA (2010) Flame retardants and organochlorine pollutants in bald eagle plasma from the Great Lakes region. Chemosphere 80:1234–1240CrossRefGoogle Scholar
  76. Verreault J, Skaare JU, Jenssen BM, Gabrielsen GW (2004) Effects of organochlorine contaminants on thyroid hormone levels in arctic breeding glaucous gulls, Larus hyperboreus. Environ Health Perspect 112:532–537CrossRefGoogle Scholar
  77. Verreault J, Letcher RJ, Ropstad E, Dahl E, Gabrielsen GW (2006) Organohalogen contaminants and reproductive hormones in incubating glaucous gulls (Larus hyperboreus) from the Norwegian Arctic. Environ Toxicol Chem 25:2990–2996CrossRefGoogle Scholar
  78. Verreault J, Helgason LB, Gabrielsen GW, Dam M, Braune BM (2013) Contrasting retinoid and thyroid hormone status in differentially-contaminated northern fulmar colonies from the Canadian Arctic, Svalbard and the Faroe Islands. Environ Int 52:29–40CrossRefGoogle Scholar
  79. Wayland M, Smits JEG, Gilchrist HG, Marchant T, Keating J (2003) Biomarker responses in nesting, common eiders in the Canadian arctic in relation to tissue cadmium, mercury and selenium concentrations. Ecotoxicology 12:225–237CrossRefGoogle Scholar
  80. Weseloh DVC, Moore DJ, Hebert CE, de Solla SR, Braune BM, McGoldrick DJ (2011) Current concentrations and spatial and temporal trends in mercury in Great Lakes herring gull eggs, 1974–2009. Ecotoxicology 20:1644–1658CrossRefGoogle Scholar
  81. Wolfe M, Norman D (1998) Effects of waterborne mercury on terrestrial wildlife at Clear Lake—evaluation and testing of a predictive model. Environ Toxicol Chem 17:214–227CrossRefGoogle Scholar
  82. Won HT, Mulvihill MJ, Wakeford BJ (2001) Multiresidue methods for the determination of chlorinated pesticides and polychlorinated biphenyls (PCBs) in wildlife tissues by gas chromatography/mass spectrometry. Technical Report Series no. 355E. Canadian Wildlife Service, Environment Canada, Hull, CanadaGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Wildlife and Landscape Science Directorate, Science and Technology BranchEnvironment and Climate Change CanadaQuébecCanada
  2. 2.Département des Sciences BiologiquesUniversité du Québec à MontréalMontréalCanada
  3. 3.Faculté de Médecine VétérinaireUniversité de MontréalSaint-HyacintheCanada

Personalised recommendations