Ecotoxicology of organochlorine chemicals in birds of the great lakes

The legacy of Rachel Carson and her now historic book Silent Spring [1] was fulfilled in the United States with passage of environmental legislation such as the Clean Water Act, the Federal Insecticide, Fungicide, and Rodenticide Act, and the Toxic Substance Control Act in the 1970s. Carson’s writings, television interviews, and testimony before Congress alerted a nation and the world to the unintended effects of persistent, bioaccumulative chemicals on populations of fish, wildlife, and possibly humans. Her writings in the popular press brought attention to scientific findings that declines in populations of a variety of birds were directly linked to the widespread use of dichlorodiphenyltrichloroethane (DDT) in agriculture, public health, and horticulture. By the 1970s, DDT and other persistent organic pollutants (POPs) were being banned or phased out, and the intent of these regulatory acts became apparent in a number of locations across the United States, including the Great Lakes. Concentrations of DDT and its major product of transformation, dichlorodiphenylchloroethane (DDE), were decreasing in top predators, such as bald eagles (Haliaeetus leucocephalus), osprey (Pandion haliaetus), colonial waterbirds, and other fish-eating wildlife [2]. Eggshell thinning and the associated mortality of bird embryos caused by DDE had decreased in the Great Lakes and elsewhere by the early 1980s [3]. Nevertheless, populations of certain species of birds in the Great Lakes were not recovering as quickly as expected. Hatching rates increased in a number of bird species; yet, fledging rates in certain populations remained low, and deformities of the bills, feet, head, and eyes were observed at elevated rates compared with populations from areas not associated with the Great Lakes or from more remote areas. Collectively, the deformities observed in a variety of fish-eating species of birds were described as Great Lakes embryo mortality and edema disease syndrome (GLEMEDS) [4]. The Canadian Wildlife Service initiated a herring gull (Larus argentatus) monitoring program in 1973 [2], partially to monitor the status and trends of concentrations or persistent residues in eggs but also to monitor biological outcomes in the birds. Meanwhile, in the United States, the U.S. Fish and Wildlife Service was also observing deformities in colonial waterbirds in certain populations they monitored, particularly in Green Bay (Lake Michigan) and Saginaw Bay (Lake Huron) (e.g., Kubiak et al. [5]). Additionally, a family of avid birders routinely visited several islands to observe and enumerate the breeding of colonial waterbirds [6]. In all cases, these monitoring efforts demonstrated that populations of most species of birds increased in the 1980s to the 1990s; but in certain locations, and particularly among colonial waterbirds, GLEMEDS continued to be observed. The causal agent(s) for the embryo deformities in select populations of Great Lakes birds had not been confirmed, but the toxicity of polychlorinated biphenyls (PCBs), chlorinated dioxins, and chlorinated furans, collectively known as dioxinlike compounds (DLCs), had been hypothesized. Discovery of the aryl hydrocarbon receptor (AhR) and then characterization of responses of several classes of chemicals that activate the AhR signal-transduction pathway in vertebrates revealed two important facts about agonists of this receptor [7]. First, similar signs of wasting syndrome (reduced weight gain), activation of hepatic oxidative enzymes (e.g., cytochrome P4501A [CYP1A]), immune suppression, and developmental anomalies (cardiovascular defects, cranial and pericardial edema, hemorrhage) were consistently observed in mammals, birds, and fish when exposed to DLCs [8]. Although sensitivity among species varies, similar AhR-mediated effects were observed following exposure to DLCs. Second, the potency of different AhR agonists to induce signs of dioxin-like toxicity followed quantitative structure–activity relationships among the different toxicological responses, leading to the development of relative toxic potency factors for DLC congeners compared to the standard, 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) [8]. The potency of individual dioxin-like congeners to induce CYP1A activity through a ligand-activated pathway and transcriptional activation of the ‘‘AhR gene battery’’ was proportionally related to the potency of that same congener to cause other pathological signs such as reduced weight gain or immune suppression [9]. These findings led to better tools for evaluating both the toxicity of DLCs and vertebrate exposure to DLCs. For example, the ability of DLCs to induce CYP1A activity in vitro could be used to evaluate the sensitivity of a particular species or to assess the toxic potency of a mixture of DLCs. Complex mixtures of DLCs could be tested and evaluated for overall toxic potency to elicit AhR-related effects using cell bioassays and responses such as ethoxyresorufin O-deethylase induction [10]. Advances in understanding the molecular signaling pathways of DLCs were critical events that allowed development of exposure-assessment tools. The subsequent marriage of these new technologies for exposure and toxicity assessment of DLCs together with intensive on-site monitoring of waterbird colonies Environmental Toxicology and Chemistry, Vol. 32, No. 3, pp. 490–492, 2013 # 2013 SETAC Printed in the USA DOI: 10.1002/etc.2109