Abstract
This study examined the associated effects of pesticides and persistent residues of p,p′-DDE on thyroid function in 16-day-old tree swallows (Tachycineta bicolor) and 12-day-old eastern bluebirds (Sialia sialis). Apple orchards sprayed with pesticides in current use and reference sites were chosen for study in southern Ontario, Canada, during 2000–2001. We assessed thyroid hormone concentrations (plasma and muscle thyroxine [T4], and triiodothyronine [T3]) and the response to a challenge with thyroid stimulating hormone (TSH) as well as parameters of thyroid histology. Individual nests were exposed to as many as seven individual pesticide applications and up to five pesticide mixtures. Concentrations of p,p′-DDE in eggs from both species were highest in orchard sites, and ranged from 0.05 to 5.44 mg/kg wet weight for tree swallows, and from 0.17 to 95.4 mg/kg for eastern bluebirds. In 2000, tree swallows from sprayed orchards had elevated plasma T4 concentrations, and thyroid glands with collapsed follicles, hypertrophic epithelia, and higher follicular epithelial cells relative to chicks from reference sites. Plasma T4 concentration was positively correlated with the total number of pesticide mixtures applied during egg incubation through chick rearing. In 2001, basal plasma T3 concentration in tree swallow chicks did not differ between orchard and reference sites, though there were differences among orchards; T3 was positively correlated with total number of individual sprays applied during egg incubation through chick rearing. Tree swallows challenged with TSH showed no significant difference in thyroid hormone concentration or follicular epithelial cell height between exposure groups; however, a significantly greater proportion of chicks from reference sites were found to have thyroids with focal or diffuse hypertrophic epithelia relative to orchard chicks. In 2001, bluebirds from sprayed orchards had significantly higher T3 concentrations in response to TSH challenge; this response was positively correlated with the total number of pesticides applied during egg incubation through chick rearing.
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References
N. Akhtar S.A. Kayani M.M. Ahmad M. Shahab (1996) ArticleTitleInsecticide-induced changes in secretory activity of the thyroid gland in rats J. Appl. Toxicol. 16 397–400 Occurrence Handle8889791 Occurrence Handle1:CAS:528:DyaK28XmtVWju7k%3D
R.A. Barter C.D. Klaassen (1992) ArticleTitleRat liver microsomal UDP-glucuronosyltransferase activity toward thyroxine: characterization, induction, and form specificity Toxicol. Appl. Pharmacol. 115 261–7 Occurrence Handle1641859 Occurrence Handle1:CAS:528:DyaK38Xlt1Gjt7c%3D
C.A. Bishop B. Collins P. Mineau N.M. Burgess W.F. Read C. Risley (2000) ArticleTitleReproduction of cavity-nesting birds in pesticide-sprayed apple orchards in southern Ontario, Canada (1988–1994) Environ. Toxicol. Chem. 19 588–99 Occurrence Handle1:CAS:528:DC%2BD3cXhtlynurk%3D
C.A. Bishop G.J. Van Der Kraak P. Ng J.E.G. Smits A. Hontela (1998) ArticleTitleHealth of tree swallows (Tachycineta bicolor) nesting in pesticide-sprayed orchards in Ontario, Canada. II. Sex and thyroid hormone concentrations and testes development J.␣Toxicol. Environ. Health. 55 531–59 Occurrence Handle1:CAS:528:DyaK1MXhtV2qsA%3D%3D
A. Brouwer D.C. Morse M.C. Lans (1998) ArticleTitleInteraction of persistent environmental organohalogens with the thyroid hormone system: mechanisms of possible consequences for animal and human health Toxicol. Ind. Health. 14 59–84 Occurrence Handle9460170 Occurrence Handle1:CAS:528:DyaK1cXjtFaltbY%3D
F. Brucker-Davis (1998) ArticleTitleEffects of environmental synthetic chemicals on thyroid function Thyroid 8 827–56 Occurrence Handle1:STN:280:DyaK1cvkvFWrtA%3D%3D Occurrence Handle9777756 Occurrence Handle10.1089/thy.1998.8.827
N.M. Burgess K.A. Hunt C. Bishop D.V. Weseloh (1999) ArticleTitleCholinesterase inhibition in tree swallows (Tachycineta bicolor) and eastern bluebirds (Sialia sialis) exposed to organophosphorus insecticides in apple orchards in Ontario, Canada Environ. Toxicol. Chem. 18 708–16 Occurrence Handle1:CAS:528:DyaK1MXitVGitrY%3D
C.C. Capen R.A. DeLellis J.T. Yarrington (2002) Endocrine system W.M. Haschek C.G. Rousseau M.A. Waalig (Eds) Handbook of Toxicologic Pathology. Academic Press San Diego 681–783
L. Chang S.L.A. Munro S.J. Richardson G. Schreiber (1999) ArticleTitleEvolution of thyroid hormone binding by transthyretins in birds and mammals Eur. J. Biochem. 259 534–42 Occurrence Handle9914537 Occurrence Handle1:CAS:528:DyaK1MXlt1Kruw%3D%3D
A.O. Cheek K. Kow J. Chen J.A. McLachlan (1999) ArticleTitlePotential mechanisms of thyroid disruption in humans: interaction of organochlorine compounds with thyroid receptor, transthyretin, and thyroid-binding globulin Environ. Health. Persp. 1074 273–8
T. Colborn (2002) ArticleTitleClues from wildlife to create an assay for thyroid system disruption Environ. Health. Persp. 110 363–7
B.K. Cooke A. Stringer (1982) ArticleTitleDistribution and breakdown of DDT in orchard soil Pestic. Sci. 13 545–51 Occurrence Handle1:CAS:528:DyaL3sXhvFegt7g%3D
C. Cox (2001) ArticleTitleImidacloprid J. Pest. Reform. 21 15–21
V.M. Darras S.P. Kotanen K.L. Geris L.R. Bergman E.R. Kühn (1996) ArticleTitlePlasma thyroid hormone levels and iodothyronine deiodinase activity following an acute glucocorticoid challenge in embryonic compared to posthatch chickens Gen. Comp. Endocrinol. 104 203–12 Occurrence Handle8930611 Occurrence Handle1:CAS:528:DyaK28XmslGjsr4%3D
V.M. Darras P. Rudas T.J. Visser T.R. Hall L.M. Huybrechts A. Vanderpooten L.R. Bergman E. Decuypere E.R. Kuhn (1993) ArticleTitleEndogenous growth hormone controls high plasma levels of 3,3,5-triiodothyronine (T3) in growing chickens by decreasing the T3-degrading type␣III deiodinase activity Domest. Anim. Endocrinol. 10 55–65 Occurrence Handle8467646 Occurrence Handle1:CAS:528:DyaK3sXktVWhtb0%3D
K.E. Deaton C.M. Bishop P.J. Butler (1998) ArticleTitleTissue-specific effects of hypothyroidism on postnatal muscle development in the barnacle goose J. Exp. Biol. 201 827–36 Occurrence Handle9464963 Occurrence Handle1:CAS:528:DyaK1cXis1Wntrc%3D
E. Decuypere C.G. Scanes E.R. Kühn (1983) ArticleTitleEffects of glucocorticoids on circulating concentrations of thyroxine (T4) and triiodothyronine (T3) and on peripheral monodeiodination in pre-and post-hatching chickens Horm. Metab. Res. 15 233–6 Occurrence Handle10.1055/s-2007-1018680 Occurrence Handle6307846 Occurrence Handle1:CAS:528:DyaL3sXkvVaksbg%3D
J.E. Elliott P.A. Martin T.W. Arnold P.H. Sinclair (1994) ArticleTitleOrganochlorines and reproductive success of birds in orchard and non-orchard areas of Central British Columbia, 1990–1991 Arch. Environ. Contam. Toxicol. 26 435–43 Occurrence Handle1:CAS:528:DyaK2cXisFajsrY%3D
K.L. Geris E. D’Hondt E.R. Kühn V.M. Darras (1999) ArticleTitleThyrotropin-releasing hormone concentrations in different regions of the chicken brain and pituitary: an ontogenic study Brain Res. 88 260–6
P.A. Gowaty J.H. Plisnner (1998) Eastern Bluebird A. Poole P. Stettenheim F. Gill (Eds) The Birds of North America. Vol. 11 Cornell Laboratory of Ornithology and The Academy of Natural Sciences Philadelphia 1–31
B. Grassle A. Biessmann (1982) ArticleTitleEffects of DDT, polychlorinated biphenyls and thiouracil on circulating thyroid hormones, thyroid histology and eggshell quality in Japanese quail (Coturnix coturnix japonica) Chem. Biol. Interact. 42 371–7 Occurrence Handle6817931 Occurrence Handle1:STN:280:DyaL3s7gtlamsw%3D%3D
C.A. Harms J.J. Hoskinson D.S. Bruyette J.W. Carpenter J. Galland J.K. Veatch S.C. Wilson J.G. Baier (1994) ArticleTitleDevelopment of an experimental model of hypothyroidism in cockatiels (Nymphicus hollandicus) Am. J. Vet. Res. 55 399–404 Occurrence Handle8192266 Occurrence Handle1:CAS:528:DyaK2cXkslyrtrs%3D
M.L. Harris L.K. Wilson J.E. Elliott C.A. Bishop K.V. Tomlin K.V. Henning (2000) ArticleTitleTransfer of DDT and metabolites from fruit orchard soils to American robins (Turdus migratorius) twenty years after agricultural use of␣DDT in Canada Arch. Environ. Contam. Toxicol. 39 205–20 Occurrence Handle10871424 Occurrence Handle1:CAS:528:DC%2BD3cXmtV2gs7Y%3D
D.J. Jefferies M.C. French (1971) ArticleTitleHyper-and hypothyroidism in pigeons fed DDT: an explanation for the ‘thin eggshell phenomenon’ Environ. Pollut. 1 235–42
D.J. Jefferies M.C. French (1972) ArticleTitleChanges induced in the pigeon thyroid by p,p′-DDE and Dieldrin J. Wildl. Manage. 36 24–30 Occurrence Handle1:CAS:528:DyaE38XhtVyru78%3D
G. Johnston G. Collet C. Walker A. Dawson I. Boyd D. Osborn (1989) ArticleTitleEnhancement of malathion toxicity to the hybrid red-legged partridge following exposure to prochloraz Pestic. Biochem. Physiol. 35 107–18 Occurrence Handle1:CAS:528:DyaK3cXitleq
G. Johnston C.H. Walker A. Dawson A. Furnell (1990) ArticleTitleInteractive effects of pesticides in the hybrid red-legged partridge Funct. Ecol. 4 309–14
G. Johnston C.H. Walker A. Dawson (1994) ArticleTitleInteractive effects between EBI fungicides (prochloraz, propiconazole and penconazole) and OP insecticides (dimethoate, chlorpyrifos, diazinon, and malathion) in the hybrid red-legged partridge Environ. Toxicol. Chem. 13 615–20 Occurrence Handle1:CAS:528:DyaK2cXis1ensLs%3D
R. Kackar M.K. Srivastava R.B. Raizada (1997) ArticleTitleStudies on rat thyroid after oral administration of mancozeb: morphological and biochemical evaluations J. Appl. Toxicol. 17 369–75 Occurrence Handle9418944 Occurrence Handle1:CAS:528:DyaK2sXotVWmsbo%3D
E.R. Kühn L.R. Bergman L. Moons F. Vandesande E. Decuypere V.M. Darras (1993) Hypothalamic and peripheral control of thyroid function during the life cycle in the chicken P.J. Sharp (Eds) Avian Endocrinology Burgess Science Press Bristol 29–45
P. Laurberg (1978) ArticleTitleNon-parallel variations in the preferential secretion of 3,5,3′-triiodothyronine (T3) and 3,3,5′-triiodothyronine (rT3) from the dog thyroid Endocrinology 102 757–66 Occurrence Handle743992 Occurrence Handle1:CAS:528:DyaE1cXhvVKkurY%3D
Mayne, G.J. (2002). Endocrine and Immune Function in Songbirds Exposed to p,p′-DDE and Current Use Pesticides in Apple Orchards. Masters Thesis, University of Guelph, Guelph, Ontario.
M.L.B. McArthur G.A. Fox D.B. Peakall B.J.R. Philogene (1983) ArticleTitleEcological significance of behavioural and hormonal abnormalities in breeding ring doves fed an organochlorine chemical mixture Arch. Environ. Contam. Toxicol. 12 343–53 Occurrence Handle6411008 Occurrence Handle1:CAS:528:DyaL3sXktVWms78%3D
F.M.A. McNabb C.G. Scanes M. Zeman (1998) Endocrine control of development J.M. Starck R.E. Ricklefs (Eds) Avian Growth and Development. Oxford University Press Oxford, UK 174–202
R.D. Moccia G.A. Fox A. Britton (1986) ArticleTitleA quantitative assessment of thyroid histopathology of herring gulls (Larus argentatus) from the Great Lakes and a hypothesis on the causal role of environmental contaminants J. Wildl. Disease. 22 60–70 Occurrence Handle1:STN:280:DyaL287ksVWksg%3D%3D
C. Nebbia J. Fink-Gremmels (1996) ArticleTitleAcute effects of low doses of zineb and ethylenethiourea on thyroid function in the male rat Bull. Environ. Contam. Toxicol. 56 847–52 Occurrence Handle8661871 Occurrence Handle1:CAS:528:DyaK28XhvVOntrs%3D
E.D. Olfert B.M. Cross A.A. McWilliams (1993) Guide to the care and use of experimental animals. Second ed. Vol 1 Canada Council on Animal Care Ottawa Ontario, Canada
B.L. Oglesbee (1992) ArticleTitleHypothyroidism in a scarlet macaw JAVMA 201 1599–1601 Occurrence Handle1289344 Occurrence Handle1:STN:280:DyaK3s7ntFWktg%3D%3D
Ontario Ministry of the Environment. (1978). The History of DDT in Ontario, Canada. Facts About Pesticides. Toronto, Ontario, Canada: Queens Printer for Ontario, Publication 10–01–02
OMAFRA (2000). Fruit Production Recommendations 2000–2001. Ontario Ministry of Agriculture, Food and Rural Affairs Toronto, Ontario, Canada: Publication 360
K. Pant A. Chandola-Saklani (1995) ArticleTitleT3 fails to mimic certain effects of T4 in munia birds: physiological implications for seasonal timing Comp. Biochem. Physiol. 111C 157–64 Occurrence Handle1:CAS:528:DyaK2MXnvFCrsbw%3D
B.D. Reinhert F.E. Wilson (1997) ArticleTitleEffects of thyroxine (T4) or triiodothyronine (T3) replacement therapy on the programming of seasonal reproduction and postnuptial molt in thyroidectomized male American tree sparrows (Spizella arborea) exposed to long days J. Exp. Zool. 279 367–76
P. Rudas G. Pethes (1984) ArticleTitleThe importance of peripheral thyroid hormone deiodination in adaptation to ambient temperature in the chicken (Gallus domesticus) Comp. Biochem. Physiol. 77 567–71
A. Siddiqui A. Baheer S.P. Srivastava (1991) ArticleTitleHeterogeneous effects of ethylene-bis-dithiocarbamate (EBDC) pesticides on oxidative metabolism of xenobiotics Pharmacol. Toxicol. 69 13–16 Occurrence Handle1946188 Occurrence Handle1:CAS:528:DyaK3MXlt12ls7Y%3D Occurrence Handle10.1111/j.1600-0773.1991.tb00401.x
N. Sinha B. Lal T.P. Singh (1991) ArticleTitlePesticide induced changes in circulating thyroid hormones in the freshwater catfish Clarias batrachus Comp. Biochem. Physiol. 100 107–10 Occurrence Handle1:STN:280:DyaK3Mzit12rsA%3D%3D
N. Sinha B. Lal T.P. Singh (1991) ArticleTitleCarbaryl-induced thyroid dysfunction in the freshwater catfish Clarias batrachus Ecotoxicol. Environ. Safe. 21 240–7 Occurrence Handle1:CAS:528:DyaK3MXksVeru7w%3D
M. Tagawa T. Hirano (1987) ArticleTitlePresence of thyroxine in eggs and changes in its content during early development of chum salmon, Oncorhynchus keta Gen. Comp. Endocrinol. 68 129–35 Occurrence Handle3666420 Occurrence Handle1:CAS:528:DyaL2sXltlWhu78%3D
J. Van Doorn F. Roelfsema D. Vander Heide (1985) ArticleTitleConcentrations of thyroxine and 3,5,3′-triiodothyronine at 34 different sites in euthyroid rats as determined by an isotopic equilibrium technique Endocrinology 117 1201–8 Occurrence Handle4017962 Occurrence Handle1:CAS:528:DyaL2MXltlGks74%3D Occurrence Handle10.1210/endo-117-3-1201
Won, H.T., Mulvihil, M.J. and Wakeford, B.J. (2001). Multiresidue methods for the determination of chlorinated pesticides and polychlorinated biphenyls (PCBs) in wildlife tissues by gas chromatography/mass spectrometry. Ottawa, Canada: Technical Report 335, Environment Canada, Canadian Wildlife Service
A.K. Yadav T.P. Singh (1986) ArticleTitleEffect of pesticide on circulating thyroid hormone levels in the freshwater catfish, Heteropneustes fossilis Environ. Res. 39 136–42 Occurrence Handle2417832 Occurrence Handle1:CAS:528:DyaL28Xhs1egtL8%3D
A.K. Yadav T.P. Singh (1987) ArticleTitlePesticide-induced impairment of thyroid physiology in the freshwater catfish, Heteropneustes fossilis Environ. Poll. 43 29–38 Occurrence Handle1:CAS:528:DyaL2sXktVagsrY%3D
J. Zar (1984) Biostatistical analysis. Second Edition Prentice Hall, Englewood Cliffs New Jersey, USA
R.D. Zenoble R.J. Kemppainen D.W. Young S.L. Clubb (1985) ArticleTitleEndocrine responses of healthy parrots to ACTH and thyroid stimulating hormone JAVMA 187 1119–20 Occurrence Handle3000999 Occurrence Handle1:CAS:528:DyaL28XktVeqsrc%3D
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Mayne, G.J., Bishop, C.A., Martin, P.A. et al. Thyroid Function in Nestling Tree Swallows and Eastern Bluebirds Exposed to Non-Persistent Pesticides and p, p′-DDE in Apple Orchards of Southern Ontario, Canada. Ecotoxicology 14, 381–396 (2005). https://doi.org/10.1007/s10646-004-6372-9
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DOI: https://doi.org/10.1007/s10646-004-6372-9