Do polychlorinated biphenyls contribute to reproduction effects in fish-eating birds?
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Associations between contaminant exposure and liver and skin tumor prevalence were evaluated in brown bullheads ( Ameiurus nebulosus ) from the tidal Potomac River, USA, watershed. Thirty bullheads (≥ age 3) were collected from Quantico embayment, near a Superfund site that released organochlorine contaminants; Neabsco Creek, a tributary with petroleum inputs from runoff and marinas; and Anacostia River (spring and fall), an urban tributary designated as a Chesapeake Bay region of concern, that was contaminated with polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), and organochlorine pesticides. Fish were collected from the Tuckahoe River, as a reference. Cytochrome P450 activity, bile PAH metabolites, and muscle organochlorine pesticide and PCB concentrations were measured in randomly selected individuals and sediment contaminants were analyzed. We found statistically significant differences in liver tumor prevalences: Anacostia (spring), 50%; Anacostia (fall), 60%; Neabsco, 17%; Quantico, 7%; and Tuckahoe, 10%. Skin tumor prevalences were significantly different: Anacostia (spring), 37%; Anacostia (fall), 10%; Neabsco, 3%; Quantico, 3%; and Tuckahoe, 0%. Tumor prevalence in Anacostia bullheads warrants concern and was similar to those at highly contaminated sites in the Great Lakes. Evidence was found of higher PAH exposure in Anacostia fish but a cause-effect linkage could not be established. Fish tumor surveys, with histopathologic examination of internal and external organs, are recommended for monitoring the status of regions of concern.
Streams receiving runoff from General Mitchell International Airport (GMIA), Milwaukee, Wisconsin, USA, were studied to assess toxic impacts of aircraft and runway deicers. Elevated levels of constituents related to deicing (propylene glycol, ethylene glycol, and ammonia) were observed in stream samples. The LC50s of type I deicer for Ceriodaphnia dubia, Pimephelas promelas, Hyalela azteca , and Chironimus tentans and the EC50 for Microtox® were less than 5,000 mg/L of propylene glycol. Concentrations up to 39,000 mg/L were observed at airport outfall sites in samples collected during deicing events. The IC25s of type I deicer for C. dubia and P. promelas were less than 1,500 mg/L of propylene glycol. Concentrations up to 960 mg/L were observed in low‐flow samples at an airport outfall site. Measured toxicity of stream water was greatest during winter storms when deicers were applied. Chronic toxicity was observed at airport outfall samples from low‐flow periods in the winter and the summer, with the greater toxic impacts from the winter sample. All forms of toxicity in stream‐water samples decreased as downstream flows increased.
Several species of anuran amphibians have undergone drastic population declines in the western United States over the last 10 to 15 years. In California, the most severe declines are in the Sierra Mountains east of the Central Valley and downwind of the intensely agricultural San Joaquin Valley. In contrast, coastal and more northern populations across from the less agrarian Sacramento Valley are stable or declining less precipitously. In this article, we provide evidence that pesticides are instrumental in declines of these species. Using Hyla regilla as a sentinel species, we found that cholinesterase (ChE) activity in tadpoles was depressed in mountainous areas east of the Central Valley compared with sites along the coast or north of the Valley. Cholinesterase was also lower in areas where ranid population status was poor or moderate compared with areas with good ranid status. Up to 50% of the sampled population in areas with reduced ChE had detectable organophosphorus residues, with concentrations as high as 190 ppb wet weight. In addition, up to 86% of some populations had measurable endosulfan concentrations and 40% had detectable 4,4′-dichlorodiphenyldichloroethylene, 4,4′-DDT, and 2,4′-DDT residues.
Energy budgets have proven to be a valuable tool for predicting life history from physiological data in terrestrial vertebrates, yet these concepts have not been applied to the physiological effects of contaminants. Contaminants might affect energy budgets by imposing an additional metabolic cost or by reducing the overall amount of energy taken in; either process will reduce the energy available for production (i.e., growth or reproduction). This study examined whole animal energetic effects of polychlorinated biphenyl (PCB) exposure in white-footed mice ( Peromyscus leucopus ). Exposure to PCBs is known to reduce concentrations of plasma thyroid hormones, and thyroid hormones exert strong control over the rate of energy metabolism in mammals. Peromyscus leucopus that were proven breeders were fed PCBs in their food at 0, 10, and 25 ppm. Through lactation, offspring were exposed to PCB from conception and were maintained on the maternal diet to adulthood. No effects were seen on energy metabolism (O 2 consumption, measured in adulthood) or on growth, but there were large dose-dependent decreases in thyroid hormone concentrations, particularly T 4 . The apparent disparity in our data between unchanged metabolic rates and 50% reductions in T 4 concentrations can be rationalized by noting that free T 3 (the fraction not bound to plasma protein) in treated mice was not significantly different from controls and that metabolism is most strongly influenced by free T 3 . Overall, this study did not demonstrate any energetic consequences of PCB exposure in P. leucopus at dietary concentrations up to 25 ppm.
We found no relationship between fish growth rate and mercury concentration in a lake trout population and conditional support for an inverse relationship in a smallmouth bass population. A bioenergetics model indicated that mercury concentration was more responsive to dietary mercury intake than to growth rate. When biodilution is evident, it may bias contaminant versus fish size relationships.
The impact of endocrine-disrupting chemicals (EDCs) has been demonstrated in mammalian models, but less research is available for avian species. The effects of vinclozolin (VIN), an antiandrogenic fungicide, on sexual differentiation and maturation were investigated in Japanese quail ( Coturnix coturnix japonica ). On day 4 of incubation, embryos were exposed to no treatment, oil, or 25, 50, or 100 ppm of VIN. Endpoints measured included adult male reproductive behavior, hypothalamic gonadotropin-releasing hormone I (GnRH-I) content in hatchlings and adults, plasma steroid levels in hatchlings and adults, proctodeal gland growth during maturation, and relative testicular weight at seven weeks of age. Results showed that exposure to VIN significantly ( p < 0.05) altered GnRH-I in male hatchlings, whereas GnRH-I levels in females remained unaffected. Although steroid levels were unaltered by any VIN treatment, the display of male reproductive behavior seemed delayed, with the number of mounts and the number of cloacal contacts being significantly ( p < 0.05) lower in the VIN-treated males. This could have an extreme negative impact on wild avian species that are routinely exposed to similar EDCs.
American kestrels ( Falco sparverius ) were fed diets containing 0 (control), 1, 3, 10, and 30 μg/g (wet wt) of Kelthane®. Residues of dicofol and its metabolites were then analyzed in the eggs and carcasses of females. Significant differences occurred among treatments for residues of both p,p ′‐dicofol and p,p ′‐dechlorodicofol (DCD) in both eggs and carcasses and for p,p ′‐dicholorbenzophenone (DCBP) in eggs. Residue concentrations increased with increasing treatment exposure. Residues of p,p ′‐dicofol, p,p ′‐DCD, and p,p ′‐DCBP in eggs were significantly correlated with eggshell quality parameters. Significant correlations also occurred among contaminants in eggs and for individual contaminants between eggs and carcasses. The lowest‐observed‐dietary‐effect concentration for eggshell thinning was 3 μg/g, whereas 1 μg/g may be considered to be near a no‐observable‐adverse‐effect concentration. Concentrations of dicofol in potential prey items and eggs of wild birds generally have been lower than dietary‐effect concentrations or concentrations in tissues or eggs associated with eggshell thinning and reduced reproductive success.
Marbled teal ( Marmaronetta angustirostris ) and white‐headed duck ( Oxyura leucocephala ) are the two European ducks threatened with global extinction. We investigated lead (Pb) poisoning in stifftails ( Oxyura spp., n = 83) and marbled teal ( n = 80) shot or found dead or moribund in Spanish wetlands via gizzard examination and liver, bone, and blood Pb analysis. Ingested Pb shot was present in 32% of shot stifftails and 70 and 43% of dead or moribund stifftails and marbled teal, respectively. Lead‐shot ingestion was more frequent in Valencia (eastern Spain), where Pb‐shot densities were higher and grit scarcer. Selection of larger grit similar in size to Pb shot may explain the higher rate of Pb‐shot ingestion observed in stifftails. Ingested shot was found more frequently in juvenile stifftails than in adults. Lead bone concentrations were higher in ducklings <9 d old than in fully grown teal and were also higher in adult than in juvenile teal. Our results show the need for a ban of Pb shot for waterfowl hunting in Spain and the cleanup of spent shot at major wetlands.
Standard environmental assessment procedures are designed to protect terrestrial and aquatic species. However, it is not known if endangered species are adequately protected by these procedures. At present, toxicological data obtained from studies with surrogate test fishes are assumed to be applicable to endangered fish species, but this assumption has not been validated. Static acute toxicity tests were used to compare the sensitivity of rainbow trout, fathead minnows, and sheepshead minnows to several federally listed fishes (Apache trout, Lahontan cutthroat trout, greenback cutthroat trout, bonytail chub, Colorado pikeminnow, razorback sucker, Leon Springs pupfish, and desert pupfish). Chemicals tested included carbaryl, copper, 4-nonylphenol, pentachlorophenol, and permethrin. Results indicated that the surrogates and listed species were of similar sensitivity. In two cases, a listed species had a 96-h LC50 (lethal concentration to 50% of the population) that was less than one half of its corresponding surrogate. In all other cases, differences between listed and surrogate species were less than twofold. A safety factor of two would provide a conservative estimate for listed cold-water, warm-water, and euryhaline fish species.
Mercury contamination in wetland biota is often dynamic, difficult to predict, and costly to track. In this paper, we present results from a six-year study of growing feathers of piscivorous birds as monitors of wetland Hg exposure in Florida, USA, wetlands. Between 1994 and 2000, we collected feathers of growing great egret ( Ardea alba ) nestlings from colonies in the freshwater Everglades of southern Florida, and during 1998, feathers were collected from chicks of both great egrets and white ibises ( Eudocimus albus ) at a variety of colonies throughout peninsular Florida. Coastal colonies showed significantly lower feather Hg concentrations than did inland sites. Within the Everglades, we found significant effects of both geographic location and year on age-adjusted mean total Hg concentrations in feathers. Over the course of our study, Everglades colonies maintained their Hg concentration rankings relative to one another, but all showed strongly declining Hg concentrations (mean of 73% averaged across colonies, between 1994 and 2000). Using a previously established predictive relationship between Hg consumption in food and feather Hg for great egrets, we estimated that Hg concentrations in the aggregate diet of egrets have been reduced by an average of 67%. We conclude that the Everglades has undergone a biologically significant decline in Hg availability in the wetland food web, possibly because of decreased local inputs.
Excess selenium (Se) in the aquatic food chain is embryotoxic and teratogenic to avocets, stilts, and other waterbirds. American avocet ( Recurvirostra americana ) and black-necked stilt ( Himantopus mexicanus ) eggs were collected from three sites in the Tulare Lake Basin of California, USA, and hatched in the laboratory. These sites included the Tulare Lake Drainage District-north (TLDD-N, water 2.5 ppb Se), TLDD-south (TLDD-S, water 8.6 ppb Se), and Westfarmers (WF, water 190 ppb Se). Highest egg Se concentrations occurred at WF (geometric mean 31.4 ppm dry wt for avocets and 20.5 ppm dry wt for stilts). Mean egg Se concentrations were 6.7 ppm for avocets and 8.4 ppm for stilts at TLDD-S, and 3.3 ppm for avocets and 2.3 ppm for stilts at TLDD-N. Hatching success and incidence of malformations did not differ among sites, but yolk sac-free hatching weights and bone lengths were less for avocets at the WF site, whereas liver weights and liver to body weight ratios were greater at that site. With increasing Se concentration, oxidative stress was most apparent in avocet hatchlings from WF: hepatic glutathione (GSH) peroxidase activity increased, glucose-6-phosphate dehydrogenase activity decreased, and oxidized glutathione (GSSG) concentration as well as the ratio of GSSG to reduced GSH concentration increased. In stilts, hepatic GSH concentration was lower in WF hatchlings. In conclusion, our findings of Se-impaired embryo growth and hepatotoxicity in avocet hatchlings suggest that oxidative stress observed in hatchlings may be related to these biological effects and may serve as a potential bioindicator of subsequent impaired functions.
The purpose of this experiment was to determine the effects of Aroclor 1242, a mixture of polychlorinated biphenyls (PCBs), on plumage characteristics and molt in the American kestrel, Falco sparverills . Several characteristics of plumage. including color and molt schedule, are modulated by hormonal signals and hence may be modified by endocrine-active contaminants. If so, the functions of plumage (e.g. communication for mating or territorial defense) may be compromised by exposure to such compounds. Captive American kestrels were fed Aroclor 1242 at 0. 6.0. and 60.0 ppm (n = 6 males and 6 females per treatment) mixed in their normal diet. Concentrations of plasma estradiol and thyroxine were measured weekly from the beginning of treatment. Measured plumage characteristics included width of the black subterminal band on the tail, color (a composite index of hue and saturation), reflectance from 230 to 800 min. pattern of feather loss and regrowth on the tail and wing. and timing of onset and duration of molt. Aroclor 1242 depressed plasma thyroxine. Plasma estradiol levels remained low due to the phase of the breeding cycle. Treatments did not disrupt the measured plumage characteristics. This may be due to timing or dose of exposure or to genetic factors.
In 1998, we collected blood samples from 63 emperor geese ( Chen canagica ) on their breeding grounds on the Yukon-Kuskokwim Delta (YKD) in western Alaska, USA. We studied the relationship between selenium concentrations in whole blood and the activities of glutathione peroxidase and glutathione reductase in plasma. Experimental studies have shown that plasma activities of these enzymes are useful biomarkers of selenium-induced oxidative stress, but little information is available on their relationship to selenium in the blood of wild birds. Adult female emperor geese incubating their eggs in mid-June had a higher mean concentration of selenium in their blood and a greater activity of glutathione peroxidase in their plasma than adult geese or goslings that were sampled during the adult flight feathermolting period in late July and early August. Glutathione peroxidase activity was positively correlated with the concentration of selenium in the blood of emperor geese, and the rate of increase relative to selenium was greater in goslings than in adults. The activity of glutathione reductase was greatest in the plasma of goslings and was greater in molting adults than incubating females but was not significantly correlated with selenium in the blood of adults or goslings. Incubating female emperor geese had high selenium concentrations in their blood, accompanied by increased glutathione peroxidase activity consistent with early oxidative stress. These findings indicate that further study of the effects of selenium exposure, particularly on reproductive success, is warranted in this species.
Depleted uranium (DU) has been used as a substitute for the fissionable enriched uranium component of atomic weapons tested at Los Alamos National Laboratory (LANL) (Los Alamos, NM, USA) since the early 1950s, resulting in considerable concentrations of DU in the soils within the test sites. Although the movement of DU into major aquatic systems has been shown to be minimal, there are many small-order ephemeral streams and areas of standing water in canyons throughout LANL that may be affected by inputs of DU via runoff, erosion, and leaching. Ninety-six-hour acute and 7-d chronic toxicity assays were conducted to measure the toxicity of DU on survival and reproduction of Ceriodaphnia dubia. A 14-d water-only assay was conducted to measure survival and growth of Hyalella azteca. The estimated median lethal concentration (LC50) to produce 50% mortality of the test population for the 96-h Ceriodaphnia dubia assay was 10.50 mg/L. Reproductive effects occurred at a lowest-observable-effect concentration ≥ 3.91 mg/L with a no-observable-effect concentration of 1.97 mg/L. The estimated 14-d LC50 for the Hyalella azteca assay was 1.52 mg/L No significant relationship was detected between growth and DU concentrations. Concentrations at which toxicity effects were observed in this study for both invertebrates exceeded concentrations of total uranium observed in runoff from LANL lands. Thus, it is likely that current runoff levels of uranium do not pose a threat to these types of aquatic invertebrates.
Pacific tree frog ( Hyla regilla ) tadpoles were collected throughout the Sierra Nevada mountain range, California, USA, in 1996 and 1997 and analyzed for the presence of polychlorinated biphenyls (PCBs) and toxaphene. Whole-tadpole Σ PCB levels ranged from 244 ng/g (wet wt) at lower elevations on the western slope to 1.6 ng/g high on the eastern slope, whereas Σ toxaphene levels ranged from 15.6 to 1.5 ng/g. Linear regression of PCB and toxaphene residue levels versus elevation indicated a significant relationship, with an r 2 value of 0.33 for PCB and 0.45 for toxaphene indicating a significant elevation effect on PCB and toxaphene bioaccumulation in Sierra Nevada H. regilla. Tadpole samples from sites in east-facing versus west-facing drainage basins showed significant differences in PCB and toxaphene residue levels, suggesting the possibility of a rain-shadow effect in the long-range atmospheric transport of these contaminants to the Sierra Nevada Mountains.
Polyhalogenated hydrocarbons have been implicated in the anomalous sexual differentiation of mammals and reptiles. Here, a temperature-sensitive turtle sex determination assay using the red-eared slider ( Trachemys scripta elegans ) was used to determine the estrogenic or antiestrogenic activity of 2,3,7,8-tetrachlorodibenzo- p -dioxin (TCDD) and 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126). Neither TCDD nor PCB-126 showed a statistically significant difference in the resulting sex ratios (Fisher's exact test, p < 0.45). As a consequence of the dosing technique (eggshell spotting), the shell retained 90 and 96% of the dose for PCB-126 and TCDD, respectively, similar to retention of estradiol-17β. However, the dosing allowed transfer of sufficient chemical to achieve tissue concentrations that were greater than most concentrations reported for environmentally incurred residues. Similar relative mass distributions of PCB-126 and TCDD were observed in albumin (14–20%), yolk (55–70%), and embryo (16–25%). Relative concentration distributions in the embryo approached those in the yolk, 37 to 40% and 40 to 52%, respectively, while relative concentrations in the albumin remained at 11 to 20%. Lipid-normalized TCDD and PCB-126 concentrations were 30- to 40-fold greater in the embryo than in the yolk. It is hypothesized that nonpassive partitioning processes may have occurred in the embryo.
Water samples were collected on three dates at 24 sites influenced by effluent from Georgia-Pacific's Palatka Pulp and Paper Mill Operation, a bleached and unbleached kraft mill near Palatka, Florida, USA. The sampling sites were located within the mill retention ponds, Rice Creek, and the St. John's River. Samples were analyzed by gas chromatography-mass spectrometry for abietic, dehydroabietic, and isopimaric acids, all of which are potentially toxic by-products of pulp production. Isopimaric acid concentrations greater than 12 mg/L were measured at the mill's effluent outfall but were less than 20 μg/L at the end of Rice Creek. This result indicates that the waters of Rice Creek provide dilution or conditions conducive for degradation or sorption of these compounds. Large differences in resin acid concentrations were observed between sampling events. In two sampling events, the maximum observed concentrations were less than 2 mg/L for each analyte. In a third sampling event, all of the compounds were detected at concentrations greater than 10 mg/L. Data from the three sample dates showed that resin acid concentrations were below 20 μg/L before the confluence of Rice Creek and the St. John's River in all cases.