Great Lakes Herring Gull Eggs Research Articles

Spatial and temporal comparisons of legacy and emerging flame retardants in herring gull eggs from colonies spanning the Laurentian Great Lakes of Canada and United States

In the Laurentian Great Lakes basin of North America, an increasing number of chemicals of emerging concern (CECs) are being investigated, including legacy and replacement flame retardants (FRs). In the present study, 14 polybrominated diphenyl ethers (PBDEs), 23 non-PBDEs halogenated FRs (NPHFRs) and 16 organophosphate ester FRs (OPE-FRs) were analyzed in 100 individual eggs collected in 2012 and 2013 and in 15 egg pools of herring gulls collected in 2012 from 20 colonies across the entire Laurentian Great Lakes basin. For CEC-FRs in eggs from all colonies, 14 PBDEs, 12 NPHFRs and 9 OPE-FRs were quantifiable in at least one of the 115 analyzed samples. The mean sum PBDE (Σ14PBDE) concentrations ranged from 244 to 657ng/g wet weight (ww), and on average were 1–2 orders of magnitude greater than the Σ12NPHFR concentrations (13.8–35.6ng/gww), and 2–3 orders of magnitude greater than Σ9OPE-FR concentrations (0.31–2.14ng/gww). Mean Σ14PBDE and sum of syn- and anti-Dechlorane Plus isomer (Σ2DDC-CO) concentrations in eggs from colonies within Laurentian Great Lakes Areas of Concern (AOCs) were in most cases greater than in eggs from nearby colonies outside of AOCs. Comparing CEC-FR concentrations in eggs collected in 2012–2013 to those previously measured in eggs collected approximately 7 years earlier (2006 and 2008) showed that Σ7PBDE (BDE-28, -47, -100, -99, -154,−153 and -183) mean concentrations in eggs from 6 colonies were approximately 30% less than they were in eggs from the same colonies from the earlier time period, whereas 3 current-use FR (BDE-209, HBCDD and Σ2DDC-CO) concentrations were significantly greater (p<0.05) than previously measured. Between 2006 and 2013 there were significant changes in individual PBDE patterns for BDE-71, -138, -153, -203, -206 and -207. Among all of the examined CEC-FRs, concentrations of Σ4PBDE (BDE-47, -99, -100 and -153) and HBCDD in gull eggs from all colonies were greater than or comparable to their lowest observed effect concentrations (LOECs) based on in ovo egg injection studies. Overall, the current profiles of a broad suite of FRs in Laurentian Great Lakes herring gull eggs highlights the need to better understand e.g., exposure-effect implications and metabolism of FRs, i.e. OPE-FRs, and emphasizes the importance of continued monitoring of CEC-FRs whose concentrations appear to be increasing, including BDE-209, HBCDD and DDC-COs.

Tetradecabromodiphenoxybenzene Flame Retardant Undergoes Photolytic Debromination

Highly brominated flame retardant compounds have relatively low bioavailability, but some of these compounds have been shown to be of environmental concern. Tetradecabromodiphenoxybenzene (TDBDPB) contains 14 bromine atoms and is the major component of commercial flame retardant mixtures such as the recently phased out SAYTEX 120. The chemical stability of TDBDPB has not been reported. We demonstrated that TDBDPB can photolytically undergo stepwise reductive debromination that follows first-order kinetic degradation models when exposed to UV or natural sunlight radiation and when dissolved in the solvents tetrahydrofuran, methanol, or n-hexane. Photolytic degradation half-lives of TDBDPB ranged from 98 to 169 min, 0.78 to 0.83 min, 1.0 to 1.8 min, and 4.9 to 7.4 min when exposed to UV-A, -B, and -C, and natural sunlight, respectively. However, the TDBDPB half-lives when exposed to UV-B and especially UV-C are likely underestimated since solutions were in borosilicate glass vials during irradiation resulting from increasingly lower % transmittance of λ < 300 nm. Neat technical TDBDPB powder exposed to UV-B and -C radiation also produced less brominated products, although the rate was much slower as compared to when in solution. Exposure of TDBDPB solutions to natural sunlight generated a number of polybrominated diphenoxybenzene (PBDPB) photolysis products, among which the Br(4)- to Br(7)-PBDPBs were the most frequently observed and estimated to be most concentrated. As evidenced by the TDBDPB half-lives and the degree of debrominated byproduct formation, the findings showed that the fraction of the absorbed irradiation that was of sufficient energy to break C-Br bonds of TDBDPB and lesser brominated PBDPBs increased from UV-B or -C to UV-A. Coincidentally, we recently reported on the presence of several Br(4) to Br(6) methoxylated PBDPBs in the Great Lakes herring gull eggs, which may be linked to a TDBDPB source via photolytic degradation to more bioavailable and persistent debromination products.

Newly Discovered Methoxylated Polybrominated Diphenoxybenzenes Have Been Contaminants in the Great Lakes Herring Gull Eggs for Thirty Years

We recently reported the discovery and identification of novel methoxylated polybrominated diphenoxybenzenes (MeO-PBDPBs) in herring gulls eggs from the Laurentian Great Lakes of North America. We presently investigated the temporal changes (1982-2010) in MeO-PBDPB concentrations and congener patterns, as well as chemical tracers of diet (ratios of carbon and nitrogen stable isotopes), in egg pool homogenates from five selected colony sites across the Great Lakes. Egg pool homogenates from the Channel-Shelter (C-S) Island (Lake Huron) contained ∑MeO-PBDPB concentrations orders of magnitude greater than those from other colonies, suggesting potential point contamination sources nearby. In the C-S Island egg pools, concentrations increased from the initial study year (31 ng/g wet weight) and peaked around the late 1990s, followed by a general decline until 2010. Over the period, concentrations generally increased in eggs from Fighting Island (Lake Erie), Toronto Harbour (Lake Ontario) and Big Sister Island (Lake Michigan) colonies, whereas the levels in Agawa Rock (Lake Superior) declined. Although other factors likely exist, changes over time in the carbon and nitrogen isotope tracers reflected a shift of the gull diet from aquatic to more terrestrial origins, and suggested this diet shift partially accounted for the temporal changes of ∑MeO-PBDPB levels in eggs from most colonies. The ratio of Br(6)- to Br(5)-MeO-PBDPB congeners generally decreased over time in the colonies at Channel-Shelter Island, Fighting Island and Agawa Rock. This suggested that Br(5)- versus Br(6)-MeO-PBDPB congeners and/or possibly their nonmethoxylated and higher brominated precursors may have been more abundant in diets of terrestrial origin. Notably, these MeO-PBDPB congeners are not "emerging" brominated substances, but rather "recently discovered" contaminants since, as of 2011, ∑MeO-PBDPB concentrations have been constantly in the range of 30-100 ng/g ww for at least the last 30 years.

Novel Methoxylated Polybrominated Diphenoxybenzene Congeners and Possible Sources in Herring Gull Eggs from the Laurentian Great Lakes of North America

An increasing number of brominated flame retardants and other brominated substances are being reported in herring gull eggs from the Laurentian Great Lakes basin. Yet, in extracts from gulls' eggs, numerous bromide anion response peaks in electron capture negative ion (ECNI) mass chromatograms remain unidentified. Using archived herring gull egg homogenates, we characterize the structures of three major and three minor, new and unique brominated substances. After extensive cleanup and separation to isolate these substances from the extracts, high-quality ECNI and electron impact (EI) mass spectra revealed fragmentation patterns consistent with congeners of methoxylated polybrominated diphenoxybenzene (MeO-PBDPB), where four congeners contained five bromines and the other two contain four and six bromines, respectively. Optimized, semiquantitative analysis revealed sum concentrations of the MeO-PBDBP congeners ranged from <0.2 to 36.8 ng/g ww in pooled egg homogenates (collected in 2009) from fourteen herring gull colony sites across the Great Lakes, with the highest concentration being for Channel-Shelter Island in Saginaw Bay (Lake Huron). To our knowledge, there are no published reports on the environmental presence and sources of MeO-PBDPBs. We hypothesize that these MeO-PBDPBs are degradation products of the polybrominated diphenoxybenzenes, for example, tetradecabromodiphenoxybenzene (currently marketed as SAYTEX 120) or polybromo 3P2E. MeO-PBDPBs in Great Lakes herring gull eggs indicates their bioaccumulation potential, and raises concerns about their origin, environmental behavior and influences on wildlife and environmental health.

Current concentrations and spatial and temporal trends in mercury in Great Lakes Herring Gull eggs, 1974–2009

Current concentrations and spatial and temporal trends of total mercury (Hg) were assessed in eggs of the Herring Gull (Larus argentatus) over the period 1974-2009 at 15 sites in the Great Lakes: 2-3 sites per lake and one site in each of 3 connecting channels. Current (2009) concentrations ranged from 0.064 μg/g (wet weight) at Chantry Island (Lake Huron) to 0.246 μg/g at Middle Island (Lake Erie). There were significant inter-colony differences in mean Hg concentrations (2005-2009). Mercury concentrations at 14 of 15 sites declined from 23 to 86% between when it was first measured (usually 1974) and 2009. Declining temporal trends over the entire period (1974-2009) were significant at 10 of the 15 sites. On the other hand, there were no significant trends in mercury over the last 15 years. In the early years, declines of Hg in Herring Gull eggs tracked those in Rainbow Smelt (Osmerus mordax) in most Great Lakes. More recently, declines in gull eggs were more evident than in smelt and may be partially explained by temporal changes in the gull diet. When gull Hg data were adjusted for temporal changes in the gull diet, as inferred from stable nitrogen isotope values in eggs, significant declines in egg mercury levels were found only at 4 of 15 sites. Overall, Hg concentrations have declined in Great Lakes Herring Gull eggs over the period 1974-2009 but changes in the gull diet may be contributing, in part, to those declines. Examination of contaminant temporal trends in multiple indicator species will ensure accurate inferences regarding contaminant availability in the environment.

2,3,4,7,8‐pentachlorodibenzofuran is a more potent cytochrome P4501A inducer than 2,3,7,8‐tetrachlorodibenzo‐p‐dioxin in herring gull hepatocyte cultures

Concentration-dependent effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 2,3,4,7,8-pentachlorodibenzofuran (PeCDF), and 2,3,7,8-tetrachlorodibenzofuran (TCDF) on cytochrome P4501A (CYP1A) induction were determined in primary cultures of embryonic herring gull (Larus argentatus) hepatocytes exposed for 24 h. Based on the concentration that induced 50% of the maximal response (EC50), the relative potencies of TCDD and TCDF did not differ by more than 3.5-fold. However, also based on the EC50, PeCDF was 40-fold, 21-fold, and 9.8-fold more potent for inducing ethoxyresorufin-O-deethylase (EROD) activity, CYP1A4 mRNA expression, and CYP1A5 mRNA expression than TCDD, respectively. The relative CYP1A-inducing potencies of PeCDF and of other dioxin-like chemicals (DLCs) in herring gull hepatocytes (HEH RePs), along with data on concentrations of DLCs in Great Lakes herring gull eggs, were used to calculate World Health Organization toxic equivalent (WHO-TEQ) concentrations and herring gull embryonic hepatocyte toxic equivalent (HEH-TEQ) concentrations. The analysis indicated that, when using avian toxic equivalency factors (TEFs) recommended by the WHO, the relative contribution of TCDD (1.1-10.2%) to total WHO-TEQ concentration was higher than that of PeCDF (1.7-2.9%). These results differ from the relative contribution of TCDD and PeCDF when HEH RePs were used; PeCDF was a major contributor (36.5-52.9%) to total HEH-TEQ concentrations, whereas the contribution by TCDD (1.2-10.3%) was less than that of PeCDF. The WHO TEFs for avian species were largely derived from studies with the domestic chicken (Gallus gallus domesticus). The findings of the present study suggest that it is necessary to determine the relative potencies of DLCs in wild birds and to re-evaluate their relative contributions to the biochemical and toxic effects previously reported in herring gulls and other avian species.

Dramatic Changes in the Temporal Trends of Polybrominated Diphenyl Ethers (PBDEs) in Herring Gull Eggs From the Laurentian Great Lakes: 1982–2006

DecaBDE is a current-use, commercial formulation of an additive, polybrominated diphenyl ether (PBDE) flame retardant composed of > 97% 2,2',3,3',4,4',5,5',6,6'-decabromoDE (BDE-209). Of the 43 PBDE congeners monitored, we report on the temporal trends (1982-2006) of quantifiable PBDEs, and specifically BDE-209, in pooled samples of herring gull (Larus argentatus) eggs from seven colonies spanning the Laurentian Great Lakes. BDE-209 concentrations in 2006 egg pools ranged from 4.5 to 20 ng/g wet weight (ww) and constituted 0.6-4.5% of sigma39PBDE concentrations among colonies, whereas sigma(octa)BDE and sigma(nona)BDE concentrations constituted from 0.5 to 2.2% and 0.3 to 1.1%, respectively. From 1982 to 2006, the BDE-209 doubling times ranged from 2.1 to 3.0 years, whereas for sigma(octa)BDEs and sigma(nona)BDEs, the mean doubling times ranged from 3.0 to 11 years and 2.4 to 5.3 years, respectively. The source of the octa- and nona-BDE congeners, e.g., BDE-207 and BDE-197, are the result of BDE-209 debromination, and they are either formed metabolically in Great Lakes herring gulls and/or bioaccumulated from the diet and subsequently transferred to their eggs. In contrast to BDE-209 and the octa- and nona-BDEs, congeners derived mainly from PentaBDE and OctaBDE mixtures, e.g., BDE-47, -99, and -100, showed rapid increases up until 2000; however, there was no increasing trend post-2000. The data illustrates that PBDE concentrations and congener pattern trends in the Great Lakes herring gull eggs have dramatically changed between 1995 and 2006. Regardless of BDE-209 not fitting the pervasive criteria as a persistent and bioaccumulative substance, it is clearly of increasing concern in Great Lake herring gulls, and provides evidence that regulation of DecaBDE formulations is warranted.

Geographical distribution (2000) and temporal trends (1981-2000) of brominated diphenyl ethers in Great Lakes hewing gull eggs.

Geographical distribution of brominated diphenyl ether (BDE) flame retardants in the North American Great Lakes ecosystem in 2000 was determined by analysis of herring gull eggs (13 egg pools) from a network of 15 monitoring colonies scattered throughout the lakes and connecting channels. sigmaBDEs were found at concentrations ranging from 192 to 1,400 microg/kg, mean of 662 +/- 368 microg/kg (wet weight of egg contents). Highest concentrations were found in northern Lake Michigan and Toronto harbor (1,000-1,400 microg/kg) and lowest in Lake Huron and Lake Erie (192-340 microg/kg). The distribution suggested that input from large urban/ industrial areas through air or water emissions contributes local contamination to the herring gull food web in addition to background levels from regional/global transport. The congener composition was similar among sampling sites. Major congeners were BDE-47 (43%), BDE-99 (26%), BDE-100 (13%) BDE-153 (11%), BDE-154 (4%), BDE-183 (2%) and BDE-28 (1%). Temporal trends of BDE contamination, 1981-2000, were established by analysis of archived herring gull eggs (10 egg pools) from colonies in northern Lake Michigan, Saginaw Bay, Lake Huron and eastern Lake Ontario. BDE-47, -99 and -100, and BDE-153, -154 and -183 concentrations were grouped separately for analysis because these two groups had different trends and are primarily associated with the Penta BDE and Octa BDE flame retardant formulations, respectively. SigmaBDE47,99,100 concentrations were 5-12 microg/kg (wet weight) in 1981-1983 and then increased exponentially (p < 0.00001) at all three sites to 400-1,100 microg/kg over the next 17 years. Doubling times were 2.6 years in Lake Michigan, 3.1 years in Lake Huron and 2.8 years in Lake Ontario. SigmaBDE154,153,183 concentrations generally increased but varied in an erratic fashion among sites and decreased as a fraction of sigmaBDE over time. Concentrations of sigmaBDE154,153,183 were 100-200 microg/kg in eggs from all three colonies in 2000. Therefore, most of the dramatic increases in sigmaBDE concentrations observed over the past 20 years in the Great Lakes aquatic ecosystem seem to be connected with the Penta BDE formulation, which is mainly used as a flame retardant in polyurethane foam in North America. If present rates of change continue, concentrations of sigmaBDEs will equal or surpass those of sigmaPCBs in Great Lakes herring gull eggs in 10-15 years.

The Ratio of DDE to PCB Concentrations in Great Lakes Herring Gull Eggs and its Use in Interpreting Contaminants Data

The ratio of DDE to PCB (DDE.PCB) concentrations was examined in herring gull ( Larus argentatus) eggs collected from thirteen sites on the Great Lakes from 1979 to 1996. This ratio has been shown to have had a number of biological interpretations in the past and the data in this study have been used to test the validity of these interpretations. The findings suggest that the consistency of DDE:PCB over many years reflects the relative availability of DDT and PCB in different geographical areas and provides an indication of a bird's general foraging ecology. The ratio can also be used as a reflection of the relative rates of increase or decrease of DDE and PCBs in food over time. A significant increase was found in the ratio in eggs sampled from sites on the upper Great Lakes and Lake Ontario during the study period. This is attributed to PCB levels decreasing faster than DDE levels at these sites. At Lake Erie and its two connecting channels, a significant increase was detected in the ratio but at a rate 56% or less than that found at other Great Lakes sites. This lower rate is attributed to DDE and PCB levels decreasing at high and equal rates. Similarities/differences in the fates of these contaminants among the Great Lakes would never have been realized upon an examination of individual contaminant levels alone. The ratio is valuable as a measure of the relative exposure of the two contaminants in non-migratory birds such as herring gulls. The use of the ratio as an indication of contamination movement through the food chain could not be assessed; the ratio cannot be used as a reflection of the interspecific differences in the accumulation and metabolism of the two contaminants. Similarities in the patterns of these ratios shown by eggs collected from sites in close proximity or within the same lake reinforce the fact that herring gulls are important as monitors of regional contaminant conditions.

Great Lakes Herring Gull Egg PCB Concentrations Indicate Approximate Steady-State Conditions

PCB concentrations in Great Lakes herring gull eggs exhibited decreases following the imposition of regulations banning PCB manufacture. However, gull egg concentrations in Lakes Superior, Michigan, Huron, and Ontario now appear to have stabilized or slightly increased. Concentrations in Lake Erie gull eggs still appearto be decreasing, though the variability in these data may limit the ability to differentiate trend changes until more data are available. This pattern is consistent with previously reported findings of stabilizing PCB concentrations in Great Lakes fishes and suggests that future improvements will be slow and difficult to discern.