A Critical Review of Bioaccumulation and Biotransformation of Organic Chemicals in Birds

A literature review of bioaccumulation and biotransformation of organic chemicals in birds was undertaken, aiming to support scoping and prioritization of future research. The objectives were to characterize available bioaccumulation/ biotransformation data, identify knowledge gaps, determine how extant data can be used, and explore the strategy and steps forward. An intermediate approach balanced between expediency and rigor was taken given the vastness of the literature. Following a critical review of \u3e500 peer-reviewed studies, \u3e25,000 data entries and 2 million information bytes were compiled on \u3e700 organic compounds for ~ 320 wild species and 60 domestic breeds of birds. These data were organized into themed databases on bioaccumulation and biotransformation, field survey, microsomal enzyme activity, metabolic pathway, and bird taxonomy and diet. Significant data gaps were identified in all databases at multiple levels. Biotransformation characterization was largely fragmented over metabolite/pathway identification and characterization of enzyme activity or biotransformation kinetics. Limited biotransformation kinetic data constrained development of an avian biotransformation model. A substantial shortage of in vivo biotransformation kinetics has been observed as most reported rate constants were derived in vitro. No metric comprehensively captured all key contaminant classes or chemical groups to support broad-scope modeling of bioaccumulation or biotransformation. However, metrics such as biota-feed accumulation factor, maximum transfer factor, and total elimination rate constant were more readily usable for modeling or benchmarking than other reviewed parameters. Analysis demonstrated the lack of bioaccumulation/biotransformation characterization of shorebirds, seabirds, and raptors. In the study of bioaccumulation and biotransformation of organic chemicals in birds, this review revealed the need for greater chemical and avian species diversity, chemical measurements in environmental media, basic biometrics and exposure conditions, multiple tissues/matrices sampling, and further exploration on biotransformation. Limitations of classical bioaccumulation metrics and current research strategies used in bird studies were also discussed. Forward-looking research strategies were proposed: adopting a chemical roadmap for future investigations, integrating existing biomonitoring data, gap-filling with non-testing approaches, improving data reporting practices, expanding field sampling scopes, bridging existing models and theories, exploring biotransformation via avian genomics, and establishing an online data repository

Affiliation in colobus vellerosus

Bibliography: p. 108-11

Field Metabolic Rate Is Dependent on Time-Activity Budget in Ring-Billed Gulls (<i>Larus delawarensis</i>) Breeding in an Anthropogenic Environment

<div><p>Environmental and behavioral factors have long been assumed to affect variation in avian field metabolic rate (FMR). However, due to the difficulties in measuring continuous behavior of birds over prolonged periods of time, complete time-activity budgets have rarely been examined in relation to FMR. Our objective was to determine the effect of activity (measured by detailed time-activity budgets) and a series of extrinsic and intrinsic factors on FMR of the omnivorous ring-billed gull (<i>Larus delawarensis</i>). The experiment was conducted during the incubation period when both members of the pair alternate between attending the nest-site and leaving the colony to forage in aquatic and anthropogenic environments (city, agricultural). FMR was determined using the doubly labeled water method. Time-activity budgets were extrapolated from spatio-temporal data (2-5 days) obtained from bird-borne GPS data loggers. Gulls had low FMRs compared to those predicted by allometric equations based on recorded FMRs from several seabird species. Gulls proportioned their time mainly to nest-site attendance (71% of total tracking time), which reduced FMR/g body mass, and was the best variable explaining energy expenditure. The next best variable was the duration of foraging trips, which increased FMR/g; FMR/g was also elevated by the proportion of time spent foraging or flying (17% and 8% of tracking time respectively). Most environmental variables measured did not impact FMR/g, however, the percent of time birds were subjected to temperatures below their lower critical temperature increased FMR. Time-activity budgets varied between the sexes, and with temperature and capture date suggesting that these variables indirectly affected FMR/g. The gulls foraged preferentially in anthropogenic-related habitats, which may have contributed to their low FMR/g due to the high availability of protein- and lipid-rich foods. This study demonstrates that activities were the best predictors of FMR/g in ring-billed gulls, thus providing strong support for this long-standing theory in bioenergetics.</p></div

Percentage of time spent in four activities by ring-billed gulls (<i>Larus delawarensis</i>).

<p>Sample size: male <i>n</i> = 19 and female <i>n</i> = 18. Data collected near Montreal (QC, Canada) during the incubation period.</p

Relationships between field metabolic rate and activity in ring-billed gulls: flying.

<p>Field metabolic rate per gram body mass was used (FMR/g). The percent of time birds spent flying is represented. Sample size: male <i>n</i> = 19 and female <i>n</i> = 18. Data collected near Montreal (QC, Canada) during the incubation period. Species: <i>Larus delawarensis</i>.</p

Relationships between field metabolic rate and activity in ring-billed gulls: Nest site attendance.

<p>Field metabolic rate per gram body mass was used (FMR/g). The percent of time birds spent in nest-site attendance is represented. Sample size: male <i>n</i> = 19 and female <i>n</i> = 18. Data collected near Montreal (QC, Canada) during the incubation period. Species: <i>Larus delawarensis</i>.</p

Relationships between field metabolic rate and activity in ring-billed gulls: Foraging.

<p>Field metabolic rate per gram body mass was used (FMR/g). The percent of time birds spent foraging is represented. Sample size: male <i>n</i> = 19 and female <i>n</i> = 18. Data collected near Montreal (QC, Canada) during the incubation period. Species: <i>Larus delawarensis</i>.</p

Transfer of hexabromocyclododecane flame retardant isomers from captive American kestrel eggs to feathers and their association with thyroid hormones and growth

Feathers are useful for monitoring contaminants in wild birds and are increasingly used to determine persistent organic pollutants. However, few studies have been conducted on birds with known exposure levels. We aimed to determine how well nestling feather concentrations reflect in ovo exposure to hexabromocyclododecane (α-, β- and γ-HBCDD), and to determine if feather concentrations are related to physiological biomarkers. Captive kestrels (n = 11) were exposed in ovo to maternally transferred HBCDD-isomers at concentrations of 127, 12 and 2 ng/g wet weight of α-, β- and γ-HBCDD (measured in sibling eggs), respectively, and compared to controls (n = 6). Nestling growth was monitored at 5 d intervals and circulating thyroid hormone concentrations assessed at d 20. Tail feathers were collected prior to the first molt and analyzed for HBCDD isomers. The mean ΣHBCDD concentration in feathers was 2405 pg/g dry weight (in exposed birds) and α-, β- and γ-HBCDD made up 32%, 13%, and 55%, respectively of the ΣHBCDD concentrations. This isomer distribution deviated from the typical dominance of α-HBCDD reported in vertebrate samples. Exposed chicks had significantly higher feather concentrations of β- and γ-HBCDD compared with controls (p = 0.007 and p = 0.001 respectively), while α-HBCDD concentrations did not differ between the two groups. Feather concentrations of α-HBCDD were best explained by egg concentrations of β- or γ-HBCDD concentrations (wi = 0.50, 0.30 respectively), while feather concentrations of β- and γ-HBCDD were influenced by growth parameters (rectrix length: wi = 0.61; tibiotarsus length: wi = 0.28). These results suggest that feather α-HBCDD concentrations may reflect internal body burdens, whereas β- and γ-HBCDD may be subject to selective uptake. The α-HBCDD concentrations in the feathers were negatively associated with the ratio of plasma free triiodothyronine to free thyroxine (T3:T4; p = 0.020), demonstrating for the first time that feather concentrations may be used to model the effect of body burdens on physiological endpoints

The Flame Retardant β‑1,2-Dibromo-4-(1,2-dibromoethyl)cyclohexane: Fate, Fertility, and Reproductive Success in American Kestrels (<i>Falco sparverius</i>)

Captive American kestrels (<i>Falco sparverius</i>) 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 (<i>p</i> = 0.019) and laid lighter eggs (successful eggs: <i>p</i> = 0.009). Exposed pairs also demonstrated poorer egg fertility (<i>p</i> = 0.035) although testis mass and histology were similar among males. Reductions in egg production and fertility resulted in decreased hatchling success (<i>p</i> = 0.023). The β-TBECH-exposed pairs also produced fewer males overall (<i>p</i> = 0.009), which occurred concurrently with increased estradiols maternally deposited in eggs (<i>p</i> = 0.039). These findings demonstrate that β-TBECH may be detrimental for breeding in wild birds receiving similar exposure levels