Timothy J. Kubiak

Great lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish‐eating birds: Similarity to chick‐edema disease

Several species of colonial fish-eating birds nesting in the Great Lakes basin, including herring gulls, common terns and double-crested cormorants, have exhibited chronic impairment of reproduction. In addition to eggshell thinning caused by high levels of DDT and metabolites, the reproductive impairment is characterized by high embryonic and chick mortality, edema, growth retardation, and deformities, hence the name Great Lakes embryo mortality, edema, and deformities syndrome (GLEMEDS). The hypothesis has been advanced that GLEMEDS in colonial fish-eating birds resembles chick-edema disease of poultry and has been caused by exposure to chick-edema active compounds that have a common mode of action through the cytochrome P-448 system. Detailed evidence has been collected from the following three groups of studies on herring gulls in the lower Great Lakes during the early 1970s; Forsters terns in Green Bay, Wisconsin in 1983; and double-crested cormorants and Caspian terns in various locations in the upper Great Lakes from 1986 onwards. It has proved difficult to establish not only the onset of the disease in the various species at various locations but also the period in which chick-edema active compounds were released. Anecdotal evidence suggested that serious egg mortality in Lake Ontario herring gulls first occurred in 1966, through the signs of chick-edema disease were not looked for until 1974. Only indirect evidence is available on the date of the release of one of the presumed causal agents, 2,3,7,8-tetrachlorodibenzo-p-dioxin, but highest levels may have occurred in the early to mid 1960s. More reliable data show that the onset of the improvement of reproduction of Lake Ontario herring gulls coincided with the declines in organochlorine compounds and particularly 2,3,7,8-TCDD and PCB. Similarly, information on the onset of the disease and exposures in the Forsters tern and double-crested cormorants in Green Bay is uncertain but bird banders did not observe deformities until the 1970s, which corresponds with the onset of high levels of PCB. If the disappearance of the Caspian tern from Saginaw Bay in the mid 1960s corresponds with the onset of GLEMEDS at that location, then there is a close temporal relationship to the onset of high PCB levels. Chick-edema disease is difficult to diagnose because there is no specific lesion, but rather there is a suite of lesions.(ABSTRACT TRUNCATED AT 400 WORDS)

Determination and occurrence of AHH-active polychlorinated biphenyls, 2,3,7,8-tetrachloro-p-dioxin and 2,3,7,8-tetrachlorodibenzofuran in Lake Michigan sediment and biota. The question of their relative toxicological significance

Abstract An analytical procedure has been developed for the determination of the 18 PCB congeners which are inducers of methylcholanthrene-like mixed function oxidase activity in animals and include the most toxic PCBs. Determinations of the toxic PCB congeners in samples of eggs of predatory fish and piscivorous birds of the Great Lakes and in Aroclor mixtures demonstrate that the apparent toxic potency of PCB residues in these samples is dominated by two congeners, 3,3′,4,4′,5- and 2,3,3′,4,4′-pentachlorobiphenyl. Furthermore, the analyses demonstrate that the potential toxicity of PCB residues can increase 5 to 10 fold as they reach upper levels of aquatic food chains and most often exceed the potential toxicity of chlorinated dibenzodioxins and furans in higher animals even in environments highly contaminated by the latter compounds.

Embryotoxicity, teratogenicity, and aryl hydrocarbon hydroxylase activity in Forster's terns on Green Bay, Lake Michigan.

Known reproductive problems, including congenital malformations and poor hatching success, exist for the state endangered Forsters tern (Sterna forsteri) in Green Bay, Wisconsin. Twenty Forsters tern eggs were collected from separate nests at a natural colony with documented reproductive problems, situated at Green Bay, Lake Michigan, and an inland colony at Lake Poygan (control) where reproduction was documented as normal. Eggs from the two locations were placed in the same laboratory incubator and candled throughout incubation. Hatching success of Green Bay eggs was 52% of that for controls. Several early embryonic deaths occurred, but most mortality occurred close to the time of hatching. Liver microsomal aryl hydrocarbon hydroxylase activity was elevated approximately threefold in Green Bay hatchlings compared to controls. Green Bay terns that hatched weighed less than controls, had an increased liver to body weight ratio, and had a shorter femur length. Two Green Bay embryos that failed to hatch had anomalies, one with a crossed beak and one with poor ossification of the foot. One Green Bay hatchling had an abnormally ossified ilium. These effects were observed in eggs where there were measureable levels of aryl hydrocarbon hydroxylase inducers including polychlorinated biphenyls and polychlorinated dibenzo-p-dioxins.

Dietary exposure of mink to carp from Saginaw Bay, Michigan. 1. Effects on reproduction and survival, and the potential risks to wild mink populations

Carp (Cyprinus carpio) collected from Saginaw Bay, Michigan, containing 8.4 mg total polychlorinated biphenyls (PCBs)/kg and 194 ng of 2,3,7,8-tetrachloro-dibenzo-p-dioxin equivalents (TEQs)/kg, were substituted for marine fish at levels of 0, 10, 20, or 40% in the diets of adult ranch mink (Mustela vison). The diets, containing 0.015, 0.72, 1.53, and 2.56 mg PCBs/kg diet, or 1.03, 19.41, 40.02, and 80.76 ng TEQs/kg diet, respectively, were fed to mink prior to and throughout the reproductive period to evaluate the effects of a naturally-contaminated prey species on their survival and reproductive performance. The total quantities of PCBs ingested by the mink fed 0, 10, 20, or 40% carp over the 85-day treatment period were 0.34, 13.2, 25.3, and 32.3 mg PCBs/mink, respectively. The corresponding quantities of TEQs ingested by the mink over the same treatment period were 23, 356, 661, and 1,019 ng TEQs/mink, respectively. Consumption of feed by mink was inversely proportional to the PCB and TEQ content of the diet. The diets containing Saginaw Bay carp caused impaired reproduction and/or reduced survival of the kits. Compared to controls, body weights of kits at birth were significantly reduced in the 20 and 40% carp groups, and kit body weights and survival in the 10 and 20% carp groups were significantly reduced at three and six weeks of age. The females fed 40% carp whelped the fewest number of kits, all of which were stillborn or died within 24 hours. Lowest observable adverse effect levels (LOAEL) of 0.134 mg PCBs/kg body weight/day or 3.6 ng TEQs/kg body weight/day for adult female mink were determined. The potential effects of exposure of wild mink to contaminated Great Lakes fish were assessed by calculating “maximum allowable daily intakes” and “hazard indices” based on total concentrations of PCB residues in several species of Great Lakes fish and mink toxicity data derived from the study.

H4IIE rat hepatoma cell bioassay-derived 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in colonial fish-eating waterbird eggs from the Great Lakes

Fish-eating waterbirds from the Great Lakes of North America have shown symptoms of poisoning similar to those observed in laboratory exposures of various avian species to planar halogenated hydrocarbons (PHHs). PHHs, include among others, polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and polychlorinated dibenzofurans (PCDFs) and have been implicated in some of the reproductive problems of Great Lakes waterbirds. The objectives of this study were to assess the overall potencies of PCB-containing extracts from colonial water-bird eggs taken from the Great Lakes and to compare the potencies with the location and spatial distribution of the colonies. The potencies of the extracts were assessed by their ability to induce cytochrome P450IA1-associated ethoxyresorufin O-deethylase (EROD) activity in H4IIE rat hepatoma cells as compared to the standard, 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). The H4IIE bioassay-derived TCDD-equivalents (TCCD-EQs) in the waterbird eggs concur with residue analyses and biological data from other studies. The greatest concentrations of TCDD-EQs were found in waterbird eggs from historically polluted, industrialized or urbanized areas in which the reproductive impairment of colonial waterbirds was most severe. However, significant concentrations of TCDD-EQs were detected at all sites tested; with a range of 49 to 415 pg TCDD-EQ/g egg, uncorrected for extraction efficiencies. The H4IIE bioassay proved to be a useful biomonitoring tool to assess the overall potency of complex PHH mixtures in environmental samples.

Contaminants in fishes from Great Lakes-influenced sections and above dams of three Michigan rivers. II: Implications for health of mink

Populations of mink (Mustela vison) have declined in many areas of the world. Such declines have been linked to exposures to synthetic, halogenated hydrocarbons. In the Great Lakes region, mink are fewer in areas along the shore of the Great Lakes and their tributaries where mink have access to fish from the Great Lakes. Recently, there has been discussion of the relative merits of passage of fishes around hydroelectric dams on rivers in Michigan. A hazard assessment was conducted to determine the potential for adverse effects on mink, which could consume such fishes from above or below dams on the rivers. Concentrations of organochlorine insecticides, polychlorinated biphenyls (PCBs), 2,3,7,8-tetrachloridibenzo-p-dioxin equivalents (TCDD-EQ), and total mercury were measured in composite samples of fishes from above or below hydroelectric dams on the Manistee and Muskegon Rivers, which flow into Lake Michigan, and the Au Sable River, which flows into Lake Huron. Concentrations of organochlorine insecticides, PCBs, and TCDD-EQ were all greater in fishes from below the dams than those from above. Concentrations of neither organochlorine insecticides nor mercury in fishes are currently a risk to mink above or below the dams. All of the species of fishes collected from downstream of the dams contained concentrations of PCBs and TCDD-EQ, which represent a hazard to mink. The hazard index for PCBs was less than one for the average of all species from the upstream reaches of the Manistee and Au Sable Rivers, but not the Muskegon. The hazard index (concentration in fish/NOAEC) was greater than 1 for all of the species collected from below the dams, in all three rivers. The greatest hazard index was observed for carp (Cyprinus carpio) downstream on the Muskegon River. Because the concentrations of PCBs used in the hazard assessment were corrected for relative toxic potencies, the hazard ratios based on PCBs should be similar to those based on TCDD-EQ. This was found to be true. Thus, either total PCBs or TCDD-EQ could be used as the critical toxicant in the hazard assessment. However, if uncorrected concentrations of PCBs, expressed as Aroclors®, were used in the hazard assessment, the toxicity of the weathered mixture would have been underestimated by approximately five-fold, and, in that instance, TCDD-EQ would be the critical contaminant for the hazard assessment. The average maximum allowable percentage of fish from above the dams, which would result in no observable adverse effects of TCDD-EQ, was 70%. Based on the average TCDD-EQ concentrations in the fishes, an average of 8.6% of the diet could be made up of fishes from below dams on the rivers. The most restrictive daily allowable intakes were for carp on the Muskegon and steelhead trout (Onchorhyncus mykiss) on the Manistee Rivers. Only 2.7% of the diet could be made up of these two species from influenced portion of the Au Sable River, they would be exposed to 390 μg PCBs and 8.55 ng of TCDD-EQ per day, respectively (Giesy et al. 1994b). Thus, it would take 15.1 or 77 days for mink to receive their total annual dose of PCBs or TCDD-EQ, respectively. At least for chinook salmon, the critical contaminant for the purposes of hazard assessment would be total concentrations of PCBs. Consuming chinook salmon for as little as 2 weeks would deliver the annual allowable dose of PCBs to mink.

Reproductive Outcomes in Colonial Fish-Eating Birds: A Biomarker for Developmental Toxicants in Great Lakes Food Chains: I. Historical and Ecotoxicological Perspectives

Colonial fish-eating birds have been used as convenient model populations in which to study the impact of chronic exposure to complex mixtures of persistent lipophilic environmental contaminants within the Great Lakes ecosystem. To date, published reports of contaminant-induced adverse reproductive outcomes exist for six species. We briefly review the studies of the herring gull (Larus argentatus), Forsters tern (Sterna forsteri), and the double-crested cormorant (Phalacrocorax auritus) to illustrate the use of reproductive outcomes in fish-eating birds as a biomarkerfor developmental toxicants in Great Lakes food chains. We discuss the management implications of using various species for such purposes. We recommend that cormorants be used more extensively in biomonitoring programs to measure exposure and effects of polyhalogenated aromatic hydrocarbons and other contaminants in aquatic food chains in the Great Lakes.

Reproductive Outcomes in Colonial Fish-Eating Birds: A Biomarker for Developmental Toxicants in Great Lakes Food Chains: II. Spatial Variation in the Occurrence and Prevalence of Bill Defects in Young Double-Crested Cormorants in the Great Lakes, 1979–1987

Abstract Congenital malformations are relatively uncommon in most wild bird populations. Here we document the occurrence of bill malformations in double-crested cormorant ( Phalacrocorax auritus ) chicks from colonies in Green Bay and elsewhere in the Great Lakes and in reference areas off the Great Lakes, in the years 1979 through 1987. In the Great Lakes, 31,168 cormorant chicks were examined during 147 visits to 42 colonies. Seventy of these chicks had crossed or deflected bills or bills in which the mandibles differed in length. Only two of the 20,962 chicks examined during 82 visits to 35 colonies in reference areas located in the prairies and northwestern Ontario had bill defects. The probability of observing a malformed chick on a visit to a colony in Green Bay was 10 to 32 times greater than on a visit to a colony in the reference areas. Bill defects were observed at only two (6%) of the colonies in the reference areas. This proportion was exceeded in six of eight geographic regions within the Great Lakes and was highest (73%) in Green Bay colonies. The prevalence of malformed chicks in Green Bay (52.1 per 10,000)was markedly greater than in all other regions during this period. These bill defects are an example of developmental asymmetry and are an indicator of developmental stability within local populations. Other investigations in Lake Michigan suggest that chemicals such as polyhalogenated aromatic hydrocarbons (e.g., PCBs) that induce aryl hydrocarbon hydroxylase are responsible for the defects observed defects.

Contaminants in fishes from great lakes-influenced sections and above dams of three Michigan Rivers. I: Concentrations of organo chlorine insecticides, polychlorinated biphenyls, dioxin equivalents, and mercury

Fishes of the Great Lakes contain hazardous chemicals such as synthetic halogenated hydrocarbons and metals. These fish can move from the lakes into the Great Lakes tributaries of Michigan. In doing so, they transport concentrationsof contaminants which may represent a risk to wildlife. Concentrations of mercury (Hg), total polychlorinated biphenyls (PCBs), 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TCDD-EQ), total DDT complex, aldrin, endrin, dieldrin, heptachlor, heptachlor epoxide, lindane, hexachlorobenzene, cis-chlordane, oxychlordane, endosulfan-I, methoxychlor, trans-chlordane, and trans-nonachlor were determined in composite samples of fishes from above and below Michigan hydroelectric dams, which separate the fishes which have access to the Great Lakes from fishes that do not. Mean concentrations of total PCBs, TCDD-EQ, DDT, and most of the other pesticides were greater in composite samples of six species of fishes from below than above the dams on the Au Sable, Manistee, and Muskegon Rivers. Concentrations of mercury, were the same or greater above the dams than below. However, this difference was statistically significant only on the Au Sable. Mercury concentrations ranged from less than 0.05 mg/kg to 0.73 mg Hg/kg, ww. Total concentrations of PCBs ranged from 0.02 to 1.7 mg/kg, ww. Concentrations of 2,3,7,8-tetrachlordibenzo-p-dioxin equivalents varied among fishes and locations. The concentrations of TCDD-EQ ranged from 2.4 to 71 μg/kg, ww, with concentrations in carp being the greatest. Concentrations of TCDD-EQ were greater than the concentrations which would be expected to occur, due solely to the presence of polychlorinated dibenzo-p-dioxins (PCDD), polychlorinated dibenzofurans (PCDF), and technical mixtures of PCBs.

Dioxin-like toxic potency in Forster's tern eggs from Green Bay, Lake Michigan, North America

Abstract The endangered Forsters tern ( Sterna forsteri ) population on Green Bay, Wisconsin has exhibited symptoms of embryotoxicity, congenital deformities, and poor hatching success. The putative causal agents are planar halogenated hydrocarbons (PHH). The objectives of this study were: 1) to evaluate the toxic potency of PHHs in extracts of Forsters tern eggs taken from Green Bay, Lake Michigan and a reference site, Lake Poygan, WI; and 2) to compare the toxic potencies of the egg extracts with the reproductive data available from the same water bird colonies. The relative toxic potency of the egg extracts was assessed with the H4IIE bioassay system to obtain 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TCDD-EQ). The average concentrations of TCDD-EQ in Forsters tern eggs were 214.5 pg/g and 23.4 pg/g from Green Bay and Lake Poygan, respectively. The bioassay results presented here concur with the biological effects and chemical analyses information from other studies on the same Forsters tern colonies.