Changes in the Incubation by American Kestrels (Falco sparverius) During Exposure to the Polybrominated Diphenyl Ether (PBDE) Mixture DE-71

Polybrominated diphenyl ethers (PBDE) are persistent environmental pollutants that have been detected in wildlife globally. American kestrels exposed to the commercial PBDE mixture DE-71 have previously demonstrated reduced reproductive success and behaviors during courtship and brood rearing; however, it remains unknown whether DE-71 affects incubation. During breeding, captive kestrels were exposed to the DE-71 mixture dissolved in safflower oil at two environmentally relevant concentrations (low: 283.5 ± 48.2, high: 1104.8 ± 124.5 ng/g wet weight [ww]) via diet for an average of 75 d. Unexpected low in ovo concentrations of hexabromocyclododecane (HBCD) were also detected (low: 3 ± 1 ng/g ww, high: 16 ± 3 ng/g ww). All comparisons are made to control pairs. Kestrel pairs in the low- and high-exposure groups experienced longer incubation periods with increasing exposure to ΣPBDE and some individual congeners. As incubation progressed, pairs exposed to DE-71 had significantly lower nest temperatures, which were on average 19% lower in low-exposure nests and 35% lower in high-exposure nests during late incubation. The DE-71 exposed pairs (low and high) also demonstrated significantly reduced incubation constancy (defined as percent of temperature readings above the maximum daily ambient temperature) during early incubation compared to controls. Nest temperatures (all pairs) and incubation constancy (high pairs) during early incubation (d 1–3) were significantly and positively associated with the proportion of eggs that hatched per pair. Higher incubation constancy and incubating nest temperatures in the low-exposure group were associated with markedly less egg weight loss by mid-incubation. These findings demonstrate that exposure to PBDE significantly affected kestrels during incubation, a critical period for embryonic development.

[1]  D. Bird,et al.  Dietary exposure to technical hexabromocyclododecane (HBCD) alters courtship, incubation and parental behaviors in American kestrels (Falco sparverius). , 2012, Chemosphere.

[2]  D. Barceló,et al.  Emerging and historical brominated flame retardants in peregrine falcon (Falco peregrinus) eggs from Canada and Spain. , 2012, Environment international.

[3]  D. Bird,et al.  Reproductive changes in American kestrels (Falco sparverius) in relation to exposure to technical hexabromocyclododecane flame retardant , 2011, Environmental toxicology and chemistry.

[4]  D. Bird,et al.  Embryonic exposure to the polybrominated diphenyl ether mixture, DE-71, affects testes and circulating testosterone concentrations in adult American kestrels (Falco sparverius). , 2011, Toxicological sciences : an official journal of the Society of Toxicology.

[5]  R. Letcher,et al.  Wastewater dilution index partially explains observed polybrominated diphenyl ether flame retardant concentrations in osprey eggs from Columbia River Basin, 2008–2009 , 2011, Ecotoxicology.

[6]  C. Henny,et al.  North American Osprey Populations and Contaminants: Historic and Contemporary Perspectives , 2010, Journal of toxicology and environmental health. Part B, Critical reviews.

[7]  D. Bird,et al.  Changes in Plasma Retinol of American Kestrels (Falco sparverius) in Response to Dietary or in Ovo Exposure to Environmentally Relevant Concentrations of a Penta-Brominated Diphenyl Ether Mixture, De-71 , 2010, Journal of toxicology and environmental health. Part A.

[8]  Robert C Hale,et al.  A global review of polybrominated diphenyl ether flame retardant contamination in birds. , 2010, Environment international.

[9]  D. Bird,et al.  Multi‐generational effects of polybrominated diphenylethers exposure: Embryonic exposure of male American kestrels (Falco sparverius) to DE‐71 alters reproductive success and behaviors , 2010, Environmental toxicology and chemistry.

[10]  J. Pérez,et al.  Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows , 2010, Proceedings of the Royal Society B: Biological Sciences.

[11]  I. Moore,et al.  Slight differences in incubation temperature affect early growth and stress endocrinology of wood duck (Aix sponsa) ducklings , 2010, Journal of Experimental Biology.

[12]  S. Bursian,et al.  Reproductive and developmental toxicity of a pentabrominated diphenyl ether mixture, DE-71, to ranch mink (Mustela vison) and hazard assessment for wild mink in the Great Lakes region. , 2009, Toxicological sciences : an official journal of the Society of Toxicology.

[13]  R. Letcher,et al.  Polybrominated diphenyl ether flame retardants in eggs may reduce reproductive success of ospreys in Oregon and Washington, USA , 2009, Ecotoxicology.

[14]  D. Bird,et al.  Environmentally relevant concentrations of DE-71 and HBCD alter eggshell thickness and reproductive success of American kestrels. , 2009, Environmental science & technology.

[15]  G. Gabrielsen,et al.  Nest temperature and parental behaviour of Arctic-breeding glaucous gulls exposed to persistent organic pollutants , 2009, Animal Behaviour.

[16]  Anders Bignert,et al.  Polybrominated diphenyl ether congener patterns, hexabromocyclododecane, and brominated biphenyl 153 in eggs of peregrine falcons (Falco peregrinus) breeding in Sweden , 2009, Environmental toxicology and chemistry.

[17]  M. L. La Guardia,et al.  Polybrominated diphenyl ethers in peregrine falcon (Falco peregrinus) eggs from the northeastern U.S. , 2008, Environmental science & technology.

[18]  J. Legler New insights into the endocrine disrupting effects of brominated flame retardants. , 2008, Chemosphere.

[19]  G. Gabrielsen,et al.  Changes in prolactin in a highly organohalogen contaminated Arctic top predator seabird, the glaucous gull. , 2008, General and comparative endocrinology.

[20]  D. Bird,et al.  Changes in reproductive courtship behaviors of adult American kestrels (Falco sparverius) exposed to environmentally relevant levels of the polybrominated diphenyl ether mixture, DE-71. , 2008, Toxicological sciences : an official journal of the Society of Toxicology.

[21]  R. Letcher,et al.  Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982-2006. , 2008, Environmental science & technology.

[22]  T. Craig American Kestrel , 2007, CRC Handbook of Census Methods for Terrestrial Vertebrates.

[23]  L. Costa,et al.  Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. , 2007, Neurotoxicology.

[24]  Yawei Wang,et al.  Polybrominated diphenyl ether in the East Asian environment: a critical review. , 2007, Environment international.

[25]  R. Letcher,et al.  Current-use flame retardants in the eggs of herring gulls (Larus argentatus) from the Laurentian Great Lakes. , 2007, Environmental science & technology.

[26]  Xiaojun Luo,et al.  Polybrominated diphenyl ethers in birds of prey from Northern China. , 2007, Environmental science & technology.

[27]  J. Mortola,et al.  Metabolic response to cooling temperatures in chicken embryos and hatchlings after cold incubation. , 2006, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[28]  L. Oring,et al.  An inexpensive method for remotely monitoring nest activity , 2006 .

[29]  Timo Hamers,et al.  In vitro profiling of the endocrine-disrupting potency of brominated flame retardants. , 2006, Toxicological sciences : an official journal of the Society of Toxicology.

[30]  P. Monaghan,et al.  Effects of early incubation constancy on embryonic development: An experimental study in the herring gull Larus argentatus , 2006 .

[31]  E. Moran,et al.  The effects of suboptimal eggshell temperature during incubation on broiler chick quality, live performance, and further processing yield. , 2006, Poultry science.

[32]  D. Bird,et al.  Behavioral variation and its consequences during incubation for American kestrels exposed to polychlorinated biphenyls. , 2006, Ecotoxicology and environmental safety.

[33]  I. Schultz,et al.  Oral exposure of PBDE-47 in fish: toxicokinetics and reproductive effects in Japanese Medaka (Oryzias latipes) and fathead minnows (Pimephales promelas). , 2006, Environmental science & technology.

[34]  K. Drouillard,et al.  Exposure to polybrominated diphenyl ethers (PBDEs): changes in thyroid, vitamin A, glutathione homeostasis, and oxidative stress in American kestrels (Falco sparverius). , 2005 .

[35]  J. Furr,et al.  In vivo and in vitro anti-androgenic effects of DE-71, a commercial polybrominated diphenyl ether (PBDE) mixture. , 2005, Toxicology and applied pharmacology.

[36]  I. Chahoud,et al.  Developmental Exposure to Low-Dose PBDE-99: Effects on Male Fertility and Neurobehavior in Rat Offspring , 2004, Environmental health perspectives.

[37]  Ronald A Hites,et al.  Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. , 2004, Environmental science & technology.

[38]  Heather M Stapleton,et al.  Polybrominated diphenyl ether flame retardants in the North American environment. , 2003, Environment international.

[39]  K. Erikstad,et al.  Patterns of incubation and nest‐site attentiveness in relation to organochlorine (PCB) contamination in glaucous gulls , 2001 .

[40]  N. French Effect of short periods of high incubation temperature on hatchability and incidence of embryo pathology of turkey eggs , 2000, British poultry science.

[41]  A. Bosveld,et al.  Effects of polyhalogenated aromatic hydrocarbons and related contaminants on common tern reproduction: Integration of biological, biochemical, and chemical data , 1996, Archives of Environmental Contamination and Toxicology.

[42]  Lawrence M. Smith,et al.  Microcontaminants and reproductive impairment of the Forster's tern on Green Bay, Lake Michigan-1983 , 1989, Archives of environmental contamination and toxicology.

[43]  R. Geers,et al.  Metabolism and growth of chickens before and after hatch in relation to incubation temperatures. , 1983, Poultry science.

[44]  B. Philogéne,et al.  Ecological significance of behavioral and hormonal abnormalities in breeding ring doves fed an organochlorine chemical mixture , 1983, Archives of environmental contamination and toxicology.

[45]  E. Kühn,et al.  Posthatch growth and development of a circadian rhythm for thyroid hormones in chicks incubated at different temperatures. , 1982, Poultry science.

[46]  D. Peakall,et al.  Behavioral Abnormalities of Nesting Lake Ontario Herring Gulls , 1978 .

[47]  D. Peakall,et al.  EFFECT OF A POLYCHLORINATED BIPHENYL ON THE REPRODUCTION OF ARTIFICIALLY AND NATURALLY INCUBATED DOVE EGGS , 1973 .

[48]  M. Eens,et al.  Brominated flame retardants and organochlorine pollutants in aquatic and terrestrial predatory birds of Belgium: levels, patterns, tissue distribution and condition factors. , 2006, Environmental pollution.

[49]  D. Deeming Avian Incubation: Behaviour, Environment, and Evolution , 2002 .

[50]  E. Olfert,et al.  Guide to the care and use of experimental animals , 1993 .