Glen A. Fox

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)

Practical causal inference for ecoepidemiologists

Environmental scientists and managers must determine whether a relationship between an environmental factor and an observed effect is causal and respond accordingly. Epidemiologists have, over the past 150 yr, developed a systematic approach to evaluating these relationships. Their criteria for objectively evaluating the relationship between a suspect cause and a chronic disease are (1) probability, (2) time order, (3) strength of association, (4) specificity, (5) consistency on replication, (6) predictive performance, and (7) coherence. These criteria can be used, with little modification, to evaluate associations in relation to diseases in fish and wildlife suspected to be caused by exposure to chemical pollutants. Some populations of fish and wildlife are members of the same guilds as subpopulations of humans. Investigations of chemically induced disease in these sentinel populations of fish and wildlife may identify the potential risks posed to these human subpopulations. Evidence evaluated using the epidemiologic criteria may assist environmental managers to determine whether a substantive case can be made to initiate preventative or remedial action. By applying the null hypothesis, scientists are forced to consider how much information must be ignored to conclude that a causal relationship does not exist.

Reproductive and Physiological Effects of Environmental Contaminants in Fish-Eating Birds of the Great Lakes: A Review of Historical Trends

During the 1950s and 1960s, reproductive failures and population declines were observed in fish-eating birds such as gulls, terns, cormorants, herons, and eagles in the Great Lakes. DDE-induced eggshell thinning contributed to these declines, but other factors such as embryo toxicity also were implicated. With reduced releases of many pollutants, reproduction recovered in some species. However, biomonitoring during the 1980s and 1990s indicates continuing effects at highly contaminated sites. Improved analytical techniques and bioassays have allowed the assessment of the total dioxin-like toxicity of complex mixtures of organochlorines (TCDD-equivalents). Developmental defects such as embryo mortality, deformities, and edema have been associated with dioxin-like PCBs in several avian species. Improved biochemical techniques have allowed the measurement of biomarkers that detect physiological alterations associated with contaminants. Specific biomarkers studied in Great Lakes birds include cytochrome P-450 monooxygenases, highly carboxylated porphyrins, thyroxine, vitamin A, and immune function. Reproductive and physiological alterations are associated with population-level effects in Caspian terns and bald eagles that feed on highly contaminated fish. Biomonitoring using biomarkers and population-level measures in fish-eating birds will continue to be important for assessing the effects of contaminants on the Great Lakes ecosystem.

Pollutant-associated embryonic mortality of great lakes herring gulls

Abstract Many embryos in recent nestings of herring gulls on Lake Ontario died prior to hatching. Signs associated with this embryonic mortality include enlarged livers, reduced embryo size, porphyria and accumulations of a subcutaneous muco-serous fluid in some embryos. These signs may be related to the widespread organochlorine pollutants DDE, dieldrin, hexachlorobenzene and PCBs.

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.

Associations between Altered Immune Function and Organochlorine Contamination in Young Caspian Terns (Sterna caspia) from Lake Huron, 1997–1999

Previous studies of laboratory animals and wildlife species have demonstrated the immunotoxicity of organochlorines. This study confirmed that associations between organochlorines and suppressed T cell function and enhanced antibody production in young Caspian terns from the Great Lakes, first observed in the early 1990s, continued into the late 1990s. These associations were based on measurement of organochlorines in plasma of individuals and pooled egg samples. During 1997–99, immune function, hematological variables, and organochlorine contamination were measured in prefledgling Caspian terns at two Lake Huron colonies: Channel Shelter Island (Confined Disposal Facility) at the mouth of the Saginaw River in southern Saginaw Bay and Elm Island in the North Channel. Elevated organochlorine exposure, reproductive effects, and decreased recruitment have been documented previously in the Saginaw Bay colony. Concentrations of polychlorinated biphenyls (PCBs) in eggs and plasma and 1,1-dichloro-2,2-bis(p)chlorophenyl)ethylene (DDE) in plasma were consistently higher in Saginaw Bay compared to the North Channel. The mean phytohemagglutinin (PHA) skin test, a measure of T lymphocyte function, was 42% lower in Saginaw Bay. Regression analyses showed strong negative associations between the PHA response and plasma PCBs and, to a slightly lesser degree, DDE. Despite interyear differences, total antibody titers following immunization with sheep red blood cells were higher in Saginaw Bay than the North Channel. Titers were positively associated with plasma PCBs and DDE. Plasma PCBs and DDE were negatively correlated with the percentage of monocytes and positively correlated with the percentage of basophils.

Ecological significance of behavioral and hormonal abnormalities in breeding ring doves fed an organochlorine chemical mixture.

Ring Doves (Streptopelia risoria) with breeding experience were fed a control diet or one of two dosages of a mixture of DDE, PCBs, mirex, and photomirex throughout an isolation period of 90 days and one reproductive cycle. Daily observations were made of courtship and parental behaviors. Circulating levels of androgens, estrogens, progesterone, thyroxine, and prolactin were measured in the appropriate sex at selected points in the breeding cycle. The organochlorine mixture altered the nature and duration of courtship behavior in a dose-related fashion resulting in marked asynchrony in the breeding cycle. Alterations were apparently mediated through the female. Incubation and brooding behavior was altered in a dose-related fashion and the median incubation period of the high dosage group was extended by three days. Pairs receiving the high dosage spent less time feeding their young. Androgen levels of males, and the estrogen and progesterone levels of females were altered in a dose-related fashion. Thyroxine levels were increased in both sexes in a dose-related fashion and there was an alteration of prolactin levels. Correlations were obtained between behavior and some hormones. There was a marked dose-related decrease in fledging success, resulting in reductions of 15 and 50% in the number of squabs fledged per nesting attempt. Squabs of pairs receiving the high dosage were of lower weight. The results suggest that behavioral anomalies in breeding synchrony, nest construction, incubation attentiveness and parental care induced in a wild bird population by a mixture of organochlorine pollutants could alter reproductive success, increase the energetic cost to the population, and alter the reproductive fitness of contaminated individuals. These effects were seen in Herring Gulls (Larus argentatus) nesting in colonies in Lake Ontario which was highly contaminated by this same suite of organochlorine pollutants in the mid-1970s.

What Have Biomarkers Told Us About the Effects of Contaminants on the Health of Fish-eating Birds in the Great Lakes? The Theory and a Literature Review

Abstract The molecular, biochemical, and cellular precursors to disease are common to wildlife and humans. Colonial fish-eating birds have been used as convenient sentinel biological systems for detection and monitoring of the effects of chronic exposure to complex mixtures of persistent toxic environmental contaminants within the Great Lakes ecosystem. Studies of impairments to health using such biomarkers as induction of mixed function oxidases, alterations in heme biosynthesis, retinol homeostasis, thyroid function and DNA integrity and various manifestations of reproductive and developmental toxicity in these birds suggests the severity varies with time and location and generally decreased between the early 1970s and late 1980s. However, these studies confirm the continued presence of sufficient amounts of PCBs and related persistent halogenated aromatic hydrocarbons in forage fish to cause physiological impairments in these birds over much of the Great Lakes basin. The elimination of such impairments will be a measures our success in remediation of Areas of Concern and “virtual elimination” of persistent polyhalogenated aromatic hydrocarbon contaminants from the Great Lakes ecosystem.

Avian thyroid development in chemically contaminated environments: is there evidence of alterations in thyroid function and development?

SUMMARY Poor reproductive success, developmental abnormalities, and behavioral alterations in fish‐eating birds in some Great Lakes areas have led to more than 35 years of toxicological studies and residue monitoring of herring gull (Larus argentatus) populations. Polyhalogenated aromatic hydrocarbons (PHAHs), especially polychlorinated biphenyls (PCBs), are widespread contaminants in the Great Lakes ecosystem. The introduction of regulations and elimination of point sources since the 1970s have resulted in decreased PHAHs in fish‐eating bird eggs and tissues. PCB exposure is associated with thyroid disruption (hypothyroidism) in mammals, but much less is known of PCB effects on avian thyroid function. Our 1998–2000 studies of herring gulls from the Great Lakes show that both pipping embryos and prefledglings from highly contaminated sites have marked depletion of thyroid gland hormone stores compared with similarly aged gulls at the reference sites. However, organismal hypothyroidism was not apparent in many embryo and chick collections where severe depletion of thyroid gland hormone was observed. Adults, sampled at two high PCB sites and a low PCB site in the Great Lakes and the maritime reference colony in 2001, showed no differences in organismal thyroid status across sites, but gulls from the high sites had enlarged thyroid glands and depressed thyroid gland hormone stores. Here we discuss the evidence that ecological exposure to PHAHs are responsible for thyroid deficiencies in gulls and that during development these deficiencies lead to developmental abnormalities in young gulls from highly contaminated Great Lakes sites.