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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.

Hexabromocyclododecane (HBCD) is a high production volume brominated flame retardant that has been detected in the environment and wildlife at increasing concentrations. This study was designed to determine potential effects of dietary exposure to environmentally relevant levels of HBCD on behavior during reproduction in captive American kestrels. Twenty kestrel pairs were exposed to 0.51 μg technical HBCD g −1 kestrel d −1 from 4 weeks prior to pairing until chicks hatched (∼75 d). Ten pairs of controls received the safflower oil vehicle only and were used for comparison. During the courtship period the chitter-calls were reduced in both sexes ( p = 0.038) and females performed fewer bonding displays ( p = 0.053). Both sexes showed a propensity to be less active than controls during courtship. The reduction in male courtship behavior was correlated with reduced courtship behaviors of females ( p ⩽ 0.008) as well as reduced egg mass ( p = 0.019). During incubation, nest temperatures of treatment pairs were lower at mid-incubation ( p = 0.038). HBCD-exposed males performed fewer key parental behaviors when rearing nestlings, including entering the nest-box, pair-bonding displays and food-retrievals. HBCD-exposed females appeared to compensate for the reduced parental behavior of their mates by performing these same behaviors more frequently than controls ( p = 0.004, p = 0.027, p = 0.025, respectively). This study demonstrates that HBCD affects breeding behavior in American kestrels throughout the reproductive season and behavioral alterations were linked to reproductive changes (egg size). This is the first study to report HBCD effects on reproductive behavior in any animal model.

Hexabromocyclododecane (HBCD) is a high-production-volume, brominated flame-retardant that is used in items such as polystyrene foams. HBCD has been detected in the environment, wildlife tissues and in humans globally with some of the highest recorded levels in predatory birds. This study examined the effects of exposure to environmentally relevant levels of HBCD on the reproductive physiology of captive male American kestrels (Falco sparverius), a predatory bird. Two sets of males were used: one group not housed with females (unpaired: nc=12, nHBCD=10) and the second group housed with females (breeding: nc=10, nHBCD=20). All treatment birds were exposed to 0.51 μg HBCD/g kestrel/day technical HBCD, and controls to safflower oil only, injected into their food during seasonal testicular development. Unpaired males were exposed for 3 weeks and euthanized for testicular analysis. Breeding males were exposed for 3 weeks prior to pairing and throughout the courtship period. The HBCD-exposed unpaired males had heavier testes (p≤0.017) and a trend towards more seminiferous tubules containing elongated spermatids (p=0.052). There was also a moderate increase in plasma testosterone concentrations (p=0.056) compared to controls. In breeding males, testosterone levels increased during courtship to culminate in higher levels than controls by the time the first egg was laid (p=0.010) and circulating free and total T4 was reduced throughout. The number of sperm cells reaching the perivitelline layer of the first egg for breeding males did not differ between the two groups. This study is the first report that HBCD exposure at environmentally relevant levels alters reproductive physiology in male birds and suggests that birds may be more sensitive to HBCD than mammals.

Polybrominated diphenyl ethers (PBDEs), a class of additive flame retardants, are temporally increasing in wildlife tissues and capable of disrupting normal endocrine function. We determined whether in ovo and post-hatch exposure of captive American kestrels (Falco sparverius) to environmentally relevant PBDEs alter thyroid, retinol, and oxidative stress measures. Control eggs were injected with safflower oil and subsequent nestlings fed the same vehicle; dosed eggs received PBDE congeners (BDE-47, -99, -100, -153), which mainly comprise the Penta-BDE commercial mixture, dissolved in safflower oil at concentrations (1500 ng/g total [Sigma] PBDEs) approximating those in Great Lakes gull eggs. Nestlings hatching from dosed eggs were orally exposed for 29 days to variable SigmaPBDE concentrations that are similar to levels reported in tissues of Great Lakes trout (100 ng/g). Treatment kestrels had lower plasma thyroxine (T(4)), plasma retinol, and hepatic retinol and retinyl palmitate concentrations, but unaltered triiodothyronine (T(3)) concentrations and thyroid glandular structure. BDE-47, -100, and -99 were negatively associated with plasma T(4), plasma retinol (BDE-100, -99) and hepatic retinol (BDE-47). Despite an antioxidant-rich diet, PBDE exposure induced hepatic oxidative stress, particularly in females, with an increased hepatic GSSG:GSH ratio, a marginal increase in lipid peroxidation, and increased oxidized glutathione. Positive associations were found between concentrations of BDE-183 and thiols and, in males, between BDE-99 and reduced GSH, but a negative association occurred between BDE-99 and TBARS. Subsequently, concentrations of PBDE congeners in wild birds may alter thyroid hormone and vitamin A concentrations, glutathione metabolism and oxidative stress.

Hexabromocyclododecane (HBCDD) is a flame retardant and a global contaminant, yet the toxicokinetics of HBCDD diastereoisomers remains unknown in wildlife species. The present study examined in captive American kestrels (Falco sparverius) (diastereo) isomer-specific HBCDD uptake, depletion, tissue distribution, and transfer to eggs in a dietary dosing study with an HBCDD technical mixture (HBCDD-TM). Adult tissue and plasma collections were from separate cohorts of unpaired individual males (n = 10) and females (n = 10) exposed for 21 d to 800 ng/g wet weight of HBCDD-TM (in safflower oil and injected into their cockerel [brain] diet), followed by a 25-d depuration period. A separate cohort of 12 males only was used for control adult tissue and plasma collections. For egg collections, separate cohorts of 11 control pairs (n = 22 birds) and 20 HBCDD-exposed pairs (n = 40 birds) were allowed to breed, and their eggs were collected (n = 19 exposed eggs and n = 10 control eggs). The sum (Σ) HBCDD concentrations were near or below detection (0.01-0.1 ng/g wet wt) in all control samples but quantifiable in all samples from exposed birds (no differences [p 0.05] between males and females). Arithmetic mean ΣHBCDD concentrations were highest in fateggsliverplasma. The mean ΣHBCDD depletion rate in plasma between the uptake and depuration periods was estimated to be 0.22 ng/g/d with a half-life of approximately 15 d. The γ-HBCDD diastereoisomer was60% of the ΣHBCDD in plasma after the uptake period and similar to the HBCDD-TM (∼80%). After the depuration period, α-HBCDD was70% of the HBCDD in plasma, fat, liver, and eggs; and this α-HBCDD domination indicated isomer-specific accumulation as a result of selective metabolism, uptake, protein binding, and/or in ovo transport.

Captive American kestrels (Falco sparverius) were exposed via diet during reproduction to an environmentally relevant concentration of β-1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (β-TBECH). The β-TBECH isomer was injected into the food source at a daily dosing concentration of 0.239 ng/g kestrel/day (22 pairs); control birds were exposed via diet to the safflower oil vehicle only (24 pairs). Eight pairs in each group were exposed for four weeks and sacrificed for tissue analysis; the remaining pairs completed their breeding cycle, with exposure ceasing at the end of incubation (82 days). α- and β-TBECH appeared to be rapidly metabolized and/or eliminated from fat, liver, and plasma; both isomers and potential hydroxylated metabolites of β-TBECH (plasma) were undetected. Notwithstanding, compared to controls, pairs exposed to β-TBECH laid fewer eggs (p = 0.019) and laid lighter eggs (successful eggs: p = 0.009). Exposed pairs also demonstrated poorer egg fertility (p = 0.035) although testis mass and histology were similar among males. Reductions in egg production and fertility resulted in decreased hatchling success (p = 0.023). The β-TBECH-exposed pairs also produced fewer males overall (p = 0.009), which occurred concurrently with increased estradiols maternally deposited in eggs (p = 0.039). These findings demonstrate that β-TBECH may be detrimental for breeding in wild birds receiving similar exposure levels.

Recently, the ban of hexabromocyclododecane (HBCD), a high-production-volume flame retardant, was announced in Europe and North America. However, the effects of HCBD remain understudied in birds. The objectives of the present comparative effects study were to determine whether exposure to an HBCD technical mixture (HBCD-TM) altered avian reproductive measures at an environmentally relevant concentration. American kestrels were exposed daily by food to HBCD-TM, i.e., 0.51 µg HBCD/g kestrel/d; exposed kestrels laid eggs that had α-HBCD concentrations (163.5 ± 75.1 ng/g wet wt) tenfold greater than β- and γ-HBCD isomers, an isomer profile and concentrations similar to those of eggs of wild peregrine falcons (Falco peregrinus). Concentrations of HBCD were not detected in the control kestrel eggs. In comparison with controls, the kestrels exposed to HBCD began to lay their eggs 6 d earlier and laid larger clutches of smaller eggs. The size of the eggs was inversely correlated with the in ovo α-HBCD concentrations. The smaller eggs of the HBCD exposed kestrels also lost more weight by midincubation, suggesting increased eggshell porosity since eggshell thickness was comparable. Generally birds that lay more eggs and lay earlier in the breeding season gain the advantage of better hatching and fledging success, yet the kestrels exposed to HBCD failed to have better reproductive success than the control birds. These reproductive changes were a function of HBCD exposure, likely through changes in food consumption, with possible impacts on, for example, reproductive behavior and/or alterations in thyroid hormones. Environ. Toxicol. Chem. 2011;30:2570–2575. © 2011 SETAC

Polybrominated diphenyl ethers (PBDEs) are additive flame retardants that are environmentally persistent and bioaccumulative. The developmental effects of in ovo exposure to environmentally relevant levels of the PBDE technical mixture, DE-71, on male reproductive physiology in captive American kestrels (Falco sparverius) was determined. Males were exposed in ovo by direct maternal transfer to DE-71 at three mean concentrations of 289 ng/g ww (low exposure), 1131 ng/g ww (high-exposure), or background levels of 3 ng/g ww (control). As adults, males were paired with unexposed females for breeding and, 1 year later, sacrificed for testes evaluation. While breeding, high-exposure males demonstrated a trend of reduced circulating testosterone levels when their female mate commenced egg laying when compared with controls (p = 0.056). No differences in circulating free T₄ or T₃ were detected. Sperm numbers were elevated on the perivitelline layer of the first egg of both high- and low-exposure males when compared with controls (p = 0.021). High-exposure males had a higher gonadosomatic index (p = 0.046) and heavier right testis than controls (p = 0.034) with a similar trend for their left testis (p = 0.055). High-exposure males had more seminiferous tubules containing lumen than controls (p = 0.030), and in proportion to the total number of tubules, low-exposure males had more tubules containing lumen than did controls (p = 0.016). Only high-exposure males had fewer than half of tubules containing final spermatids (43%). The results of the present study demonstrate that embryonic exposure to technical DE-71 affects the reproductive tract of adult male kestrels.

Polybrominated diphenyl ethers (PBDEs) and total alpha-hexabromocyclododecane (HBCD) are flame-retardant additives that are commonly used in household and commercial applications. PBDE congeners, which are comprised of technical mixtures such as DE-71, are globally persistent and their concentrations are increasing in many species. Captive American kestrels (Falco sparverius) were exposed by diet to vehicle (safflower oil), or one of two environmentally relevant concentrations of DE-71 and unintentionally to HBCD. This exposure resulted in the birds laying eggs that contain PBDE and HBCD concentrations currently found in wild herring gull (Larus argentatus) and peregrine falcon (F. peregrinus) eggs, and compared to control kestrels, resulted in delayed egg laying and smaller eggs being laid, caused thinner eggshells and differential weight loss during embryonic development, and reduced fertility and reproductive success. The thickness of the eggshell declined as the concentrations of all measured PBDE and the total amount of a-HBCD congeners (except BDE-183 and BDE-209) increased; increasing concentrations of BDE-153, BDE-154, BDE-28, BDE-17, delayed egg laying, reduced eggshell mass (plus sigmaPBDEs), and reduced fledging success (BDE-153 and BDE-154 only). BDE-153 is the dominant congener recently found in peregrine eggs. The results of this study are consistent with the PBDE-associated brood reduction in wild European peregrines and may partially explain the decline of kestrels in North America.

Polybrominated diphenyl ether (PBDEs) concentrations are increasing exponentially in biota. We studied the growth of American kestrel ( Falco sparverius ) nestlings exposed in ovo and during development to environmentally relevant PBDE congeners and concentrations. Eggs within each clutch, divided between groups by laying sequence, were injected into the air cell at 19 days of incubation with safflower oil or penta-BDE congeners BDE-47, -99, -100, and -153 dissolved in safflower oil (18.7 μg total [Σ] PBDEs/egg), approximating current levels in Great Lakes herring gulls. The measured proportions of BDE congeners found in the dosing oil were 56.4% of BDE-47; 27.2% of BDE-99; 24.8% of BDE-100; and 0.6% of BDE-153. For 29 days, nestlings were orally gavaged daily with the same ΣPBDE mixture (15.6 ± 0.3 ng/g body weight/day). Relative congener abundances in the dosing mixture compared to the carcasses suggest biotransformation of BDE-47; BDE-183 was also detected. PBDE exposure did not affect hatching or fledging success. PBDE-exposed nestlings were larger (weight, bones, feathers) as they gained weight more quickly and ate more food, the latter in association with their ΣPBDE body burdens. BDE-100 was most influential on nestling growth, being positively associated with size, weight gain, and food consumption. Increasing concentrations of BDE-183 and -153 were related to longer bones, and BDE-99 to longer feathers. The larger size of the PBDE-exposed birds may be detrimental to their bone structure and have excessive energetic costs. The repeated relationships with BDE-100 and growth may be important for wild Falconidae , since this is the predominant penta-BDE congener in these raptors. Copyright© Taylor & Francis Group, LLC.