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

Abstract

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; Forster's 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, though 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 Forster's 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. GLEMEDS is characterized by an elevated incidence of embryonic and chick mortality, growth retardation, and developmental abnormalities, including bill deformities, club feet, missing eyes, and defective feathering, and there is also subcutaneous, percardial, and peritoneal edema, liver enlargement, liver necrosis, and porphyria. These signs conform to the known symptoms of chick‐edema disease. A variety of chick‐edema active compounds, including non‐ortho‐substituted PCBs and dibenzo‐p‐dioxins and furans substituted at the lateral positions, produce chick‐edema disease. The active compounds have specific conformational requirements. In considering evidence on the strength of association, the embryos and chicks of herring gulls from Lake Ontario and Forster's terns from Creen Bay had a significant increase in the incidence of the lesions compared to the reference colonies. Similarly, the incidence of bill abnormalities was significantly elevated in Great Lakes colonies of double‐crested cormorants particularly for Green Bay, Wisconsin. There was a significant dose‐response relationship between the incidence of embryonic mortality in cormorant eggs and the presence of chick‐edema active compounds expressed in 2,3,7,8‐TCDD equivalents. There is a high degree of consistency on replication. The disease has been found in a variety of species in a variety of locations, by different observers using different study designs. Outbreaks of the disease have occurred at different times and seem only to be related to exposures of developing embryos to high levels of chick‐edema active compounds. The new facts, that embryos and chicks of colonial, fish‐eating birds can exhibit signs resembling chick‐edema disease when exposed to chick‐edema active compounds, cohere with existing biological theory, experience, and experimentation. There are plausible routes of exposure and sources of these compounds to the Great Lakes, and statistically significant dose‐response relationships have been demonstrated.