Investigating endocrine and physiological parameters of captive American kestrels exposed by diet to selected organophosphate flame retardants.

Organophosphate triesters are high production volume additive flame retardants (OPFRs) and plasticizers. Shown to accumulate in abiotic and biotic environmental compartments, little is known about the risks they pose. Captive adult male American kestrels (Falco sparverius) were fed the same dose (22 ng OPFR/g kestrel/d) daily (21 d) of tris(2-butoxyethyl) phosphate (TBOEP), tris(2-chloroethyl) phosphate (TCEP), tris(2-chloroisopropyl) phosphate (TCIPP), or tris(1,2-dichloro-2-propyl) phosphate (TDCIPP). Concentrations were undetected in tissues (renal, hepatic), suggesting rapid metabolism. There were no changes in glutathione status, indicators of hepatic oxidative status, or the cholinergic system (i.e., cerebrum, plasma cholinesterases; cerebrum muscarinic, nicotinic receptors). Modest changes occurred in hepatocyte integrity and function (clinical chemistry). Significant effects on plasma free triiodothyronine (FT3) concentrations occurred with exposure to TBOEP, TCEP, TCIPP, and TDCIPP; TBOEP and TCEP had additional overall effects on free thyroxine (FT4), whereas TDCIPP also influenced total thyroxine (TT4). Relative increases (32%-96%) in circulating FT3, TT3, FT4, and/or TT4 were variable with each OPFR at 7 d exposure, but limited thereafter, which was likely maintained through decreased thyroid gland activity and increased hepatic deiodinase activity. The observed physiological and endocrine effects occurred at environmentally relevant concentrations and suggest parent OPFRs or metabolites may have been present despite rapid degradation.

Snapping Turtles (Chelydra serpentina) from Canadian Areas of Concern across the southern Laurentian Great Lakes: Chlorinated and brominated hydrocarbon contaminants and metabolites in relation to circulating concentrations of thyroxine and vitamin A.

The metabolites of polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs), as well as other halogenated phenolic contaminants (HPCs) have been shown to have endocrine-disrupting properties, and have been reported with increasing frequency in the blood of wildlife, and mainly in mammals and birds. However, little is known about the persistence, accumulation and distribution of these contaminants in long-lived freshwater reptiles. In the present study, in addition to a large suite of chlorinated and brominated contaminants, metabolites and HPCs, we assessed and compared hydroxylated (OH) PCBs and OH-PBDEs relative to PCBs and PBDEs, respectively, in the plasma of adult male common snapping turtles (Chelydra serpentina). Blood samples were collected from 62 snapping turtles (2001-2004) at 12 wetland sites between the Detroit River and the St. Lawrence River on the Canadian side of the Laurentian Great Lakes of North America. Turtles were sampled from sites designated as Areas of Concern (AOCs) and from a relatively clean reference site in southern Georgian Bay (Tiny Marsh), Lake Huron. Plasma concentrations of Σ46PCB (10-340 ng/g wet weight (ww)) and Σ28OH-PCB (3-83 ng/g ww) were significantly greater (p<0.05) in turtles from the Turkey Creek and Muddy Creek-Wheatley Harbour sites in Lake Erie compared with the reference site turtles. The HPC, pentachlorophenol (PCP), had a mean concentration of 9.6±1.1 ng/g ww. Of the 28 OH-CB congeners screened for, 4-OH-CB187 (42±7 ng/g ww) was the most concentrated of all HPCs measured. Of the 14 OH-BDE congeners examined, four (4'-OH-BDE17, 3-OH-BDE47, 5-OH-BDE47 and 4'-OH-BDE49) were consistently found in all plasma samples. p,p'-DDE was the most concentrated of the 18 organochlorine pesticides (OCPs) examined. The mean concentrations of circulating total thyroxine (TT4), dehydroretinol and retinol in the plasma of the male snapping turtles regardless of sampling site were 5.4±0.3, 81±4.7 and 291±13 ng/mL, respectively. Significant (p<0.05) negative (e.g. cis-chlordane) or positive (e.g. BDE-99) correlations between some of the target contaminants and TT4, dehydroretinol or retinol were observed. To our knowledge, we report for the first time on HPC (e.g. OH-PCBs) and methylsulfonyl- (MeSO2-) PCB metabolite contaminants in the plasma of any freshwater turtle or freshwater reptilian species. Our findings also show that the accumulation of OH-PCBs, MeSO2-PCBs, OH-PBDEs and some OCPs in the snapping turtles from Lake Erie and Lake Ontario (in 2001-2004) had the potential for eliciting endocrine disruption. Exposure to these contaminants and associated adverse effects on the endocrine system in freshwater reptiles and the related mechanisms require further investigation.

Waste-water treatment plants are implicated as an important source of flame retardants in insectivorous tree swallows (Tachicyneta bicolor).

Wastewater treatment plants (WWTPs) are an important source of anthropogenic chemicals, including organic flame retardants (FRs). Limited studies indicate birds can be exposed to FRs by feeding from waters receiving WWTP effluent or in fields receiving biosolids. Expanding on our earlier study, 47 legacy and 18 new FR contaminants were characterized in the eggs of insectivorous tree swallows (Tachycineta bicolor) feeding in water bodies receiving effluent from two WWTPs and compared to those from a reference site 19 km downstream of the nearest WWTP. Of the FRs measured, polybrominated diphenyl ethers (PBDEs) dominated the FR profile, specifically BDE-47, -99, -100, -153, -154, with considerably lower concentrations of hexabromocyclododecane (HBCDD), BDE-183 and BDE-209; each detected in 96-100% of the eggs overall except HBCDD (83%). FR concentrations were usually significantly greater in eggs from the secondary WWTP versus the tertiary WWTP and/or reference site. Despite low detection rates, concentrations of new FRs, specifically pentabromobenzyl acrylate (PBBA), 1,2,-bis-(2,4,6-tribromophenoxy)ethane (BTBPE), bis(2-ethylhexyl)-tetrabromophthalate (BEHTBP), tetrabromo-o-chlorotoluene (TBCT), hexabromobenzene (HBB), α- and ß-1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane (DBE-DBCH), were greater than HBCDD or BDE-209. Additional evidence that WWTPs are an important source of exposure to new FR contaminants for birds utilizing associated water bodies is that only the WTTP eggs, not the reference eggs, had measureable concentrations of PBBA, TBCT, BEHTBP, HBB, α-DBE-DBCH, 2,2',4,5,5'-pentabromobiphenyl (BB-101), pentabromoethyl benzene (PBEB), 2,4,6-tribromophenyl allyl ether (TBPAE), and tetrabromo-p-xylene (pTBX). Our study suggests that WWTPs are an important source of legacy and new FR contaminants for birds consuming prey that are associated with WWTP out-flows.

Bioaccumulation and biotransformation of 61 polychlorinated biphenyl and four polybrominated diphenyl ether congeners in juvenile American kestrels (Falco sparverius).

This study examined the bioaccumulation and dietary retention of 61 polychlorinated biphenyl (PCB) and four polybrominated diphenyl ether (PBDE) congeners in juvenile American kestrels (Falco sparverius). American kestrels were exposed to contaminants via egg injection and daily gavage dosing over the posthatch-to-fledgling period. Retention factors for PCBs were dependent on chemical hydrophobicity and chlorine substitution patterns and ranged from less than 1 to 16.4% for PCBs having vicinal hydrogen substitutions at meta-, para- carbons on at least one of the phenyl rings and between 13.2 and 81.5% for congeners containing chlorine substitutions at 4,4'-, 3',4,5'-, 3,4',5-, or 3,3',5,5'-positions. These results indicate that juveniles are capable of biotransforming PCBs according to the same structure-activity rules as adults. A toxicokinetic model, initially parameterized using adult toxicokinetic parameters, was used to describe concentration trends in juveniles over time. The adult model overestimated PCB concentrations but provided an adequate fit when elimination rate constants were increased by a factor of 12.7. Retention factors for the PBDE congeners 2,2',4,4'-tetrabromodiphenyl ether (BDE 47), 2,2',4,4',6-pentabromodiphenyl ether (BDE 100), 2,2',4,4',5-pentabromodiphenyl ether (BDE 99), and 2,2',4,4',5,5'-hexabromodiphenyl ether (BDE 153) were from 7.8 to 45.3% of the total dose. The retention of BDE 47 was similar that observed for readily cleared PCBs, whereas the remaining PBDEs exhibited retention factors consistent with those of persistent PCBs. Half-lives for PBDEs in juveniles were estimated to range from 5.6 to 44.7 d. Assuming differences in PBDE toxicokinetics between juveniles and adults similar to those measured for PCBs, adult American kestrel PBDE half-lives are expected to range from 72 to 572 d.

Effects of environmentally relevant concentrations of atrazine on gonadal development of snapping turtles (Chelydra serpentina).

The herbicide atrazine has been suspected of affecting sexual development by inducing aromatase, resulting in the increased conversion of androgens to estrogens. We used snapping turtles (Chelydra serpentina), a species in which sex is dependent on the production of estrogen through aromatase activity in a temperature-dependent manner, to investigate if environmentally relevant exposures to atrazine affected gonadal development. Eggs were incubated in soil to which atrazine was applied at a typical field application rate (3.1 L/ha), 10-fold this rate (31 L/ha), and a control rate (no atrazine) for the duration of embryonic development. The incubation temperature (25 degrees C) was selected to produce only males. Although some males with testicular oocytes and females were produced in the atrazine-treated groups (3.3-3.7%) but not in the control group, no statistical differences were found among treatments. Furthermore, snapping turtle eggs collected from natural nests in a corn field were incubated at the pivotal temperature (27.5 degrees C) at which both males and females normally would be produced, and some males had oocytes in the testes (15.4%). The presence of low numbers of males with oocytes may be a natural phenomenon, and we have limited evidence to suggest that the presence of normal males with oocytes may represent a feminizing effect of atrazine. Histological examination of the thyroid gland revealed no effect on thyroid morphology.

Exposure to the androgenic brominated flame retardant 1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane alters reproductive and aggressive behaviors in birds.

Detected in environmental samples, 1,2-dibromo-4-(1,2-dibromoethyl) cyclohexane (DBE-DBCH) is a bioaccumulative isomer of a current-use brominated flame retardant. All 4 structural isomers are androgen agonists; however, little toxicological information exists for this compound. The objective of the present study was to determine if ß-DBE-DBCH, the isomer found most prominently in animal tissue, affects androgen-dependent behavior of breeding American kestrels (Falco sparverius). The authors hypothesized that if ß-DBE-DBCH acts as an androgen agonist in kestrels, androgen-dependent behaviors (i.e., copulation, courtship, aggression) would increase and behaviors inhibited by androgens (i.e., parental care behaviors) would decrease. Sixteen captive experimental kestrel pairs were exposed to 0.239 ng ß-DBE-DBCH/g kestrel/d by diet from 4 wk prior to pairing until their nestlings hatched (mean 82 d) and compared with vehicle only-exposed control pairs (n = 15). Androgen-dependent behaviors were significantly increased in ß-DBE-DBCH-exposed birds, consistent with the authors' hypothesis. These behavioral changes included copulation and other sexual behaviors in males and females and aggression in males, suggesting that ß-DBE-DBCH may have acted like an androgen agonist in these birds. Parental behaviors were not reduced in exposed birds as predicted, although dietary exposure had ceased before chicks hatched. Further assessment of ß-DBE-DBCH is recommended given these behavioral changes and the previously reported reproductive changes in the same birds.

Characterization of contaminants in snapping turtles (Chelydra serpentina) from Canadian Lake Erie Areas of Concern: St. Clair River, Detroit River, and Wheatley Harbour.

PCBs, organochlorine pesticides and dioxins/furans in snapping turtle eggs and plasma (Chelydra serpentina) were evaluated at three Areas of Concern (AOCs) on Lake Erie and its connecting channels (St. Clair River, Detroit River, and Wheatley Harbour), as well as two inland reference sites (Algonquin Provincial Park and Tiny Marsh) in 2001-2002. Eggs from the Detroit River and Wheatley Harbour AOCs had the highest levels of p,p'-DDE (24.4 and 57.9 ng/g) and sum PCBs (928.6 and 491.0 ng/g) wet weight, respectively. Contaminant levels in eggs from St. Clair River AOC were generally higher than those from Algonquin Park, but similar to those from Tiny Marsh. Dioxins appeared highest from the Detroit River. The PCB congener pattern in eggs suggested that turtles from the Detroit River and Wheatley Harbour AOCs were exposed to Aroclor 1260. TEQs of sum PCBs in eggs from all AOCs and p,p'-DDE levels in eggs from the Wheatley Harbour and the Detroit River AOCs exceeded the Canadian Environmental Quality Guidelines. Furthermore, sum PCBs in eggs from Detroit River and Wheatley Harbour exceeded partial restriction guidelines for consumption. Although estimated PCB body burdens in muscle tissue of females were well below consumption guidelines, estimated residues in liver and adipose were above guidelines for most sites.

Avian wildlife as sentinels of ecosystem health.

Birds have been widely used as sentinels of ecosystem health reflecting changes in habitat quality, increased incidence of disease, and exposure to and effects of chemical contaminants. Numerous studies addressing these issues focus on the breeding period, since hormonal, behavioural, reproductive, and developmental aspects of the health can be observed over a relatively short time-span. Many body systems within individuals are tightly integrated and interdependent, and can be affected by contaminant chemicals, disease, and habitat changes in complex ways. Animals higher in the food web will reflect cumulative effects of multiple stressors. Such features make birds ideal indicators for assessing environmental health in areas of environmental concern. Five case studies are presented, highlighting the use of different species which have provided insight into ecosystem sustainability, including (i) the consequences of anthropogenic disturbances of sagebrush habitat on the greater northern sage grouse Centrocercus urophasianus; (ii) the high prevalence of disease in very specific passerine species in the Canary Islands closely paralleling deterioration of formerly productive desert habitat and ensuing interspecific stressors; (iii) fractures, abnormal bone structure, and associated biochemical aberrations in nestling storks exposed to acidic tailings mud from a dyke rupture at an iron pyrite mine near Sevilla, Spain; (iv) newly presented data demonstrating biochemical changes in nestling peregrine falcons Falco peregrinus and associations with exposure to major chemical classes in the Great Lakes Basin of Canada; and (v) the variability in responses of tree swallows Tachycineta bicolor to contaminants, biological and meteorological challenges when breeding in the Athabasca oil sands.