Wastewater dilution index partially explains observed polybrominated diphenyl ether flame retardant concentrations in osprey eggs from Columbia River Basin, 2008-2009.

Several polybrominated biphenyl ether (PBDE) congeners were found in all 175 osprey (Pandion haliaetus) eggs collected from the Columbia River Basin between 2002 and 2009. ΣPBDE concentrations in 2008-2009 were highest in osprey eggs from the two lowest flow rivers studied; however, each river flowed through relatively large and populous metropolitan areas (Boise, Idaho and Spokane, Washington). We used the volume of Wastewater Treatment Plant (WWTP) discharge, a known source of PBDEs, as a measure of human activity at a location, and combined with river flow (both converted to millions of gallons/day) created a novel approach (an approximate Dilution Index) to relate waterborne contaminants to levels of these contaminants that reach avian eggs. This approach provided a useful understanding of the spatial osprey egg concentration patterns observed. Individual osprey egg concentrations along the Upper Willamette River co-varied with the Dilution Index, while combined egg data (geometric means) from rivers or segments of rivers showed a strong, significant relationship to the Dilution Index with one exception, the Boise River. There, we believe osprey egg concentrations were lower than expected because Boise River ospreys foraged perhaps 50-75% of the time off the river at ponds and lakes stocked with fish that contained relatively low ΣPBDE concentrations. Our limited temporal data at specific localities (2004-2009) suggests that ΣPBDE concentrations in osprey eggs peaked between 2005 and 2007, and then decreased, perhaps in response to penta- and octa-PBDE technical mixtures no longer being used in the USA after 2004. Empirical estimates of biomagnification factors (BMFs) from fish to osprey eggs were 3.76-7.52 on a wet weight (ww) basis or 4.37-11.0 lipid weight. Our earlier osprey study suggested that ΣPBDE egg concentrations >1,000 ng/g ww may reduce osprey reproductive success. Only two of the study areas sampled in 2008-2009 contained individual eggs with ΣPBDE concentrations >1,000 ng/g, and non-significant (P > 0.30) negative relationships were found between ΣPBDEs and reproductive success. Additional monitoring is required to confirm not only the apparent decline in PBDE concentrations in osprey eggs that occurred during this study, but also to better understand the relationship between PBDEs in eggs and reproductive success.

North American osprey populations and contaminants: historic and contemporary perspectives.

Osprey (Pandion haliaetus) populations were adversely affected by DDT and perhaps other contaminants in the United States and elsewhere. Reduced productivity, eggshell thinning, and high DDE concentrations in eggs were the signs associated with declining osprey populations in the 1950s, 1960s, and 1970s. The species was one of the first studied on a large scale to bring contaminant issues into focus. Although few quantitative population data were available prior to the 1960s, many osprey populations in North America were studied during the 1960s and 1970s with much learned about basic life history and biology. This article reviews the historical and current effects of contaminants on regional osprey populations. Breeding populations in many regions of North America showed post-DDT-era (1972) population increases of varying magnitudes, with many populations now appearing to stabilize at much higher numbers than initially reported in the 1970s and 1980s. However, the magnitude of regional population increases in the United States between 1981 (first Nationwide Survey, ∼8,000 pairs), when some recovery had already occurred, 1994 (second survey, ∼14,200), and 2001 (third survey, ∼16,000-19,000), or any other years, is likely not a simple response to the release from earlier contaminant effects, but a response to multi-factorial effects. This indirect "contaminant effects" measurement comparing changes (i.e., recovery) in post-DDT-era population numbers over time is probably confounded by changing human attitudes toward birds of prey (shooting, destroying nests, etc.), changing habitats, changing fish populations, and perhaps competition from other species. The species' adaptation to newly created reservoirs and its increasing use of artificial nesting structures (power poles, nesting platforms, cell towers, channel markers, offshore duck blinds, etc.) are two important factors. The timing of the initial use of artificial nesting structures, which replaced declining numbers of suitable trees at many locations, varied regionally (much later in the western United States and Mexico). Because of the increasing use of artificial nesting structures, there may be more ospreys nesting in North America now than ever before. Now, with the impact of most legacy organic contaminants (DDT, other organochlorine [OC] pesticides, polychlorinated biphenyls [PCB], polychlorinated dibenzo-p-dioxins [PCDD], polychlorinated dibenzofurans (PCDF]) greatly reduced or eliminated, and some osprey populations showing evidence of stabilizing, the species was proposed as a Worldwide Sentinel Species for evaluating emerging contaminants. Several emerging contaminants are already being studied, such as polybrominated diphenyl ethers (PBDE) and perfluorinated acids and sulfonate compounds (PFC). The many advantages for continued contaminant investigations using the osprey include a good understanding of its biology and ecology, its known distribution and abundance, and its ability to habituate to humans and their activities, which permits nesting in some of the potentially most contaminated environments. It is a top predator in most ecosystems, and its nests are relatively easy to locate and study with little researcher impact on reproductive success.

Polybrominated diphenyl ether flame retardants in eggs may reduce reproductive success of ospreys in Oregon and Washington, USA.

Spatial and temporal assessments and reports of polybrominated diphenyl ether (PBDE) flame retardants in birds remain sparse. In the present study, PBDEs were detected in all 120 osprey (Pandion haliaetus) eggs collected. The eggs were collected from nests along the Columbia, Willamette and Yakima rivers of Oregon (OR) and Washington (WA) and in Puget Sound (WA) between 2002 and 2007. PBDE congeners: 17, 28, 47, 49, 66, 85, 99, 100, 138, 153, 154 (possible coelution with brominated biphenyl 153 [BB153]), 183, 190 (detected in one egg), 209 (not detected), and BB101 (only detected in 2006 and 2007) and total-alpha-hexabromocyclododecane (only detected in five eggs) were analyzed for in the egg samples. Eggs from reservoirs in the forested headwaters of the Willamette River (2002) contained the lowest concentrations of SigmaPBDEs (geometric mean [range], 98 [55.2-275] ng/g wet weight [ww]), while those from the middle Willamette River (2006) contained the highest (897 [507-1,880] ng/g ww). Concentrations in eggs from the Columbia River progressively increased downstream from Umatilla, OR (River Mile [RM] 286) to Skamokoa, WA (RM 29), which indicated additive PBDE sources along the river. In general, regardless of the year of egg collection, differences in PBDE concentrations reported in osprey eggs along the three major rivers studied (Columbia, Willamette and Yakima) seem to reflect differences in river flow (dilution effect) and the extent of human population and industry (source inputs) along the rivers. PBDE concentrations increased over time at two locations (Seattle, WA; Columbia River, RM 29-84) where temporal patterns could be evaluated. Only during 2006 (on the middle Willamette River, RM 61-157) and 2007 (on the lower Columbia River, RM 29-84) did SigmaPBDE concentrations in osprey eggs exceed 1,000 ng/g ww with negative relationships indicated at both locations between productivity and SigmaPBDE concentrations in eggs (P = 0.008, P = 0.057). Osprey eggs from Everett, WA contained nearly twice the SigmaPBDE concentration (geometric mean 239 vs. 141 ng/g ww, range 124-384 vs. 22.2-819 ng/g ww, P < or = 0.05) as double-crested cormorant (Phalacrocorax auritus) eggs collected at the same location and time, which is likely due to dietary differences. No significant relationship (all Ps > 0.147) was indicated between PBDE congeners (including SigmaPBDEs) and eggshell thickness at the concentrations observed in this study.

Osprey: worldwide sentinel species for assessing and monitoring environmental contamination in rivers, lakes, reservoirs, and estuaries.

In the United States, many fish and wildlife species have been used nationwide to monitor environmental contaminant exposure and effects, including carcasses of the bald eagle (Haliaeetus leucocephalus), the only top avian predator regularly used in the past. Unfortunately, bald eagles are sensitive to investigator intrusion at the nest. Thus, the osprey (Pandion haliaetus) is evaluated as a potential sentinel species for aquatic ecosystems. Several characteristics support the choice of the osprey as a sentinel species, including: (1) fish-eating diet atop the aquatic food web, (2) long-lived with strong nest fidelity, (3) adapts to human landscapes (potentially the most contaminated), (4) tolerates short-term nest disturbance, (5) nests spatially distributed at regular intervals, (6) highly visible nests easily located for study, (7) ability to accumulate most, if not all, lipophilic contaminants, (8) known sensitivity to many contaminants, and (9) nearly a worldwide distribution. These osprey traits have been instrumental in successfully using the species to understand population distribution, abundance, and changes over time; the effects of various contaminants on reproductive success; how contaminants in prey (fish on biomass basis) contribute to egg concentrations (i.e., biomagnification factors); and spatial residue patterns. Data summarized include nesting population surveys, detailed nesting studies, and chemical analyses of osprey egg, organ, blood, and feather samples for contaminants that bioaccumulate and/or biomagnify in aquatic food webs; and biochemical evaluations of blood and various organs. Studies in the United States, Canada, Mexico, Europe, and elsewhere have shown the osprey to be a useful sentinel species for monitoring selected environmental contaminants, including some emerging contaminants in lakes, reservoirs, rivers, and estuaries.

Mercury and drought along the lower Carson river, Nevada: III. Effects on blood and organ biochemistry and histopathology of snowy egrets and Black-crowned night-herons on Lahontan reservoir, 2002-2006.

A 10-year study (1997-2006) was conducted to evaluate reproduction and health of aquatic birds in the Carson River Basin of northwestern Nevada (on the U.S. Environmental Protection Agency Natural Priorities List) due to high mercury (Hg) concentrations from past mining activities. This part of the study evaluated physiological associations with blood Hg in young snowy egrets (Egretta thula) and black-crowned night-herons (Nycticorax nycticorax), and organ biochemistry and histopathological effects in snowy egrets on Lahontan Reservoir (LR) from the period 2002-2006. LR snowy egret geometric mean total Hg concentrations (microg/g ww) ranged from 1.5 to 4.8 for blood, 2.4 to 3.1 liver, 1.8 to 2.5 kidneys, 1.7 to 2.4 brain, and 20.5 to 36.4 feathers over these years. For night-herons, mean Hg for blood ranged from 1.6 to 7.4. Significant positive correlations were found between total Hg in blood and five plasma enzyme activities of snowy egrets suggesting hepatic stress. Histopathological findings revealed vacuolar changes in hepatocytes in LR snowy egrets as well as correlation of increased liver inflammation with increasing blood and tissue Hg. Hepatic oxidative effects were manifested by decreased hepatic total thiol concentration and glutathione reductase activity and elevated hepatic thiobarbituric acid-reactive subatances (TBARS), a measure of lipid peroxidation. However, other hepatic changes indicated compensatory mechanisms in response to oxidative stress, including decreased oxidized glutathione (GSSG) concentration and decreased ratio of GSSG to reduced glutathione. In young black-crowned night-herons, fewer correlations were apparent. In both species, positive correlations between blood total Hg and plasma uric acid and inorganic phosphorus were suggestive of renal stress, which was supported by histopathological findings. Both oxidative effects and adaptive responses to oxidative stress were apparent in kidneys and brain. Vacuolar change and inflammation in peripheral nerves were found to correlate with blood and tissue Hg. Hg-associated effects related to the immune system included alterations in specific white blood cells and lymphoid depletion in the bursa that were correlated with blood and tissue Hg. When the number of plasma variables that differed between young snowy egrets from the LR site and the reference site were compared between wet and drought years, over twice as many variables were affected during drought years. This resulted in many more variables correlating with blood total Hg during dry than during wet years, suggesting the combination of drought and Hg was more stressful than Hg alone. Drought may have exacerbated Hg-related effects as reported previously for overall productivity. This relationship was not evident in black-crowned night-herons, although data were more limited.

PCDDs, PCDFs, PCBs, OC pesticides and mercury in fish and osprey eggs from Willamette River, Oregon (1993, 2001 and 2006) with calculated biomagnification factors.

The osprey (Pandion haliaetus) population nesting along the main stem Willamette River and lower Santiam River was first studied to evaluate contaminants and reproductive rates in 1993 when 78 occupied nests were present. By 2001, the population increased to 234 occupied nests, a 13.7% annual rate of population increase. A sample egg was collected from each of a series of nests along the Upper River (river mile 55-187) in 1993, 2001 and 2006 to evaluate trends of persistent contaminants (organochlorine [OC] pesticides, polychlorinated biphenyls [PCBs], polychlorinated dibenzo-p-dioxins [PCDDs], and polychlorinated dibenzofurans [PCDFs]). Nearly all OC pesticide residues decreased significantly, e.g., p, p'-DDE (DDE) from 2,350 to 1,353 to 210 microg/kg wet weight (ww). PCBs followed a similar pattern over time, e.g., SigmaPCBs 688 to 245 to 182 microg/kg ww, while PCDDs and PCDFs showed a more precipitous decline (often 85-95%) between 1993 and 2001, with no egg analyses warranted in 2006. During 2001-2002, sample osprey eggs were also collected from nests at three Headwater Reservoirs and two lower reaches (Newberg Pool and Tidal Portland) of the Willamette River, as well as the lower portion of the Santiam River to evaluate spatial residue patterns. Significant differences were seldom detected among the different sampling areas for OC pesticides (probably due to small sample sizes), although higher concentrations were often seen in the lower reaches, e.g., DDE 901 microg/kg ww (Headwater Reservoirs), 1,353 (Upper River), 1,384 (Newberg Pool) and 2,676 (Tidal Portland). PCB congener concentrations in eggs were usually higher in the Tidal Portland reach than at other locations and often significantly higher than at the Headwater Reservoirs or Upper River. Mercury (first analyzed in eggs in 2001), PCDDs and PCDFs were extremely low in 2001/2002 with no significant spatial patterns. Whole fish composite samples of largescale sucker (Catastomus macrocheilus) and northern pikeminnow (Ptychocheilus oregonensis), which account for about 90% of the biomass in the diet of this osprey population, were also collected from the Willamette River in 1993 and 2001 and analyzed for the same contaminants as osprey eggs. Contaminant residues in fish from the Upper River decreased between 1993 and 2001, paralleling findings for osprey eggs. Likewise, spatial patterns for fish residues paralleled findings for osprey eggs from the different reaches in 2001. A second empirical estimate of biomagnification factors (BMFs) from fish to osprey eggs for OC pesticides, PCBs, PCDDs and PCDFs (ww and lipid weight [lw] basis) was calculated based on residue data collected in 2001. The two independent BMF estimates (1993 and 2001) for each contaminant from the Upper River provide a measure of consistency, e.g., DDE (ww) 87 and 79, (lw) 103 and 112; SigmaPCBs (ww) 11 and 8.4, (lw) 13 and 12. Mercury did not biomagnify from fish to osprey eggs (BMF = 0.60). Legacy contaminants investigated had limited (perhaps only DDE), if any, effects on reproductive success of the increasing osprey population nesting along the Willamette River by 2001.

Dacthal and chlorophenoxy herbicides and chlorothalonil fungicide in eggs of osprey (Pandion haliaetus) from the Duwamish-Lake Washington-Puget Sound area of Washington state, USA.

Current-use chlorophenoxy herbicides including 2,4-dichlorophenoxyacetic acid, dicamba, triclopyr, dicamba, dimethyl tetrachloroterephthalate (DCPA or dacthal), and the metabolite of pyrethroids, 3-phenoxybenzoic acid (3-PBA), and the fungicide, chlorothalonil, were investigated in the eggs of osprey (Pandion haliaetus) that were collected from 15 sites from five study areas Puget Sound/Seattle area of Washington State, USA. DCPA differs from acidic chlorophenoxy herbicides, and is not readily hydrolyzed to free acid or acid metabolites, and thus we developed a new method. Of the 12 chlorophenoxy herbicides and chlorothalonil analyzed only DCPA could be quantified at six of these sites (2.0 to 10.3 pg/g fresh weight). However, higher levels (6.9 to 85.5 pg/g fresh weight) of the unexpected DCPA structural isomer, dimethyl tetrachlorophthalate (diMe-TCP) were quantified in eggs from all sites. diMe-TCP concentrations tended to be higher in eggs from the Everett Harbor area. As diMe-TCP is not an industrial product, and not commercially available, the source of diMe-TCP is unclear. Regardless, these findings indicate that DCPA and diMe-TCP can be accumulated in the food chain of fish-eating osprey, and transferred in ovo to eggs, and thus may be of concern to the health of the developing chick and the general reproductive health of this osprey population.

Assessing mercury exposure and effects to American dippers in headwater streams near mining sites.

To evaluate mercury (Hg) exposure and possible adverse effects of Hg on American dipper (Cinclus mexicanus) reproduction, we collected eggs and nestling feathers and the larval/nymph form of three Orders of aquatic macroinvertebrates (Ephemeroptera, Plecoptera and Trichoptera = EPT) important in their diet from three major headwater tributaries of the upper Willamette River, Oregon in 2002. The Coast Fork Willamette River is contaminated with Hg due to historical cinnabar (HgS) mining at the Black Butte Mine; the Row River is affected by past gold-mining operations located within the Bohemia Mining District, where Hg was used in the amalgamation process to recover gold; and the Middle Fork Willamette River is the reference area with no known mining. Methyl mercury (MeHg) concentrations (geometric mean) in composite EPT larvae (111.9 ng/g dry weight [dw] or 19.8 ng/g wet weight [ww]), dipper eggs (38.5 ng/g ww) and nestling feathers (1158 ng/g ww) collected from the Coast Fork Willamette were significantly higher than MeHg concentrations in EPT and dipper samples from other streams. Total mercury (THg) concentrations in surface sediments along the same Hg-impacted streams were investigated by others in 1999 (Row River tributaries) and 2002 (Coast Fork). The reported sediment THg concentrations paralleled our biological findings. Dipper breeding territories at higher elevations had fewer second clutches; however, dipper reproductive success along all streams (including the lower elevation and most Hg-contaminated Coast Fork), was judged excellent compared to other studies reviewed. Furthermore, MeHg concentrations in EPT samples from this study were well below dietary concentrations in other aquatic bird species, such as loons and ducks, reported to cause Hg-related reproductive problems. Our data suggest that either dipper feathers or EPT composites used to project MeHg concentrations in dipper feathers (with biomagnification factor of 10-20x) may be used, but with caution, to screen headwater streams for potential Hg-related effects on dippers. When actual feather concentrations or projected feather concentrations are equal to or lower than concentrations reported for the Coast Fork, dippers are expected to reproduce well (assuming adequate prey and suitable nest sites). When Hg concentrations are substantially higher, more detailed investigations may be required. Birds feeding almost exclusively on fish (e.g., osprey [Pandion haliaetus]) and usually found further downstream from the headwaters would not be adequately represented by dippers given the higher MeHg concentrations in fish resulting from biomagnification, compared to lower trophic level invertebrates.

Biomagnification factors (fish to Osprey eggs from Willamette River, Oregon, U.S.A.) for PCDDs, PCDFs, PCBs and OC pesticides.

A migratory population of 78 pairs of Osprey (Pandion haliaetus) nesting along the Willamette River in western Oregon was studied in 1993. The study was designed to determine contaminant concentrations in eggs, contaminant concentrations in fish species predominant in the Ospreys diet, and Biomagnification Factors (BMFs) of contaminants from fish species eaten to Osprey eggs. Ten Osprey eggs and 25 composite samples of fish (3 species) were used to evaluate organochlorine (OC) pesticides, polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and polychlorinated dibenzofurans (PCDFs). Mercury was also analyzed in fish. Geometric mean residues in Osprey eggs were judged low, e.g., DDE 2.3 microg g(-1) wet weight (ww), sigma PCBs 0.69 microg g(-1), 2,3,7,8-TCDD 2.3 ng kg(-1), and generally well below known threshold values for adverse effects on productivity, and the population was increasing. Osprey egg residue data presented by River Mile (RM) are discussed, e.g., higher PCDDs were generally found immediately downstream of paper mills and eggs from the Willamette River had significantly elevated PCBs and PCDDs compared to reference eggs collected nearby in the Cascade Mountains. Prey remains at nest sites indicated that the Largescale Sucker (Catostomus macrocheilus) and Northern Pikeminnow (Ptychocheilus oregonensis) accounted for an estimated 90.1% of the biomass in the Osprey diet, and composite samples of these two species were collected from different sampling sites throughout the study area for contaminant analyses. With the large percentage of the fish biomass in the Osprey diet sampled for contaminants (and fish eaten by Ospreys similar in size to those chemically analyzed), and fish contaminant concentrations weighted by biomass intake, a mean BMF was estimated from fish to Osprey eggs for the large series of contaminants. BMFs ranged from no biomagnification (0.42) for 2,3,7,8-TCDF to 174 for OCDD. Our findings for the migratory Osprey were compared to BMFs for the resident Herring Gull (Larus argentatus), and differences are discussed. We believe a BMF approach provides some basic understanding of relationships between contaminant burdens in prey species of fish-eating birds and contaminants incorporated into their eggs, and may prove useful in understanding sources of contaminants in migratory species although additional studies are needed.