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

Abstract

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.

Effects of organochlorine contaminants on thyroid hormone levels in Arctic breeding glaucous gulls, Larus hyperboreus.

“…The T 4 :T 3 ratio is known to be altered by changing iodine availability where high iodine favors T 4 formation (increasing T 4 :T 3 ratio), and low iodine favors T 3 formation (decreasing T 4 :T 3 ratio; McNabb 1992). However, studies on fish-eating birds such as the herring gull (Larus argentatus) from the Great Lakes in North America have provided strong evidence that hypothyroidism in this species was due not to iodine deficiency but to exposure to halogenated organic contaminants, although the disruptive mechanisms suggested were speculative (Fox 1993;McNabb and Fox 2003;Moccia et al 1986). Based on these results, and because marine environments (e.g., the Barents Sea) are documented to be rich in iodine compared with freshwater environments (e.g., the Great Lakes; Fox 1993; Peakall 1992), iodine deficiency is not likely to occur in glaucous gulls breeding at Bear Island.…”

“…As yet, exceedingly few studies have been performed on competition between halogenated organic contaminants, especially compounds such as HCB and oxychlordane, and THs for binding sites on TTR and albumin in avian species. Other possible mechanisms for contaminant-induced modulation of thyroid functions and T 4 turnover have been reported in diverse reviews (e.g., Leatherland 2000;McNabb and Fox 2003;Peakall 1992). …”

Polychlorinated biphenyl effects on avian hepatic enzyme induction and thyroid function

“…Some of these developmental abnormalities include defects of the central nervous system and skeletal anomalies, such as incomplete skeletal ossification and stunted growth. For instance, embryos of fish-eating birds collected at contaminated sites in the Great Lakes had shorter femur and tarsal lengths than those collected at reference sites (reviews, Fox, 1993;McNabb and Fox, 2003;Scanes and McNabb, 2003).…”

“…These chemicals are lipophilic, so they are stored in body fats and biomagnify up the food chain, increasing exposure in top predators such as fish-eating birds. In addition, female birds deposit these chemicals in their eggs, exposing their young as embryos, when they may be most vulnerable to toxicants (reviews, McNabb and Fox, 2003;Scanes and McNabb, 2003).…”

“…In wildlife such as fish-eating birds, polychlorinated biphenyls (PCBs) have been associated with developmental abnormalities that may be due to altered thyroid function (reviews, Fox, 1993;McNabb and Fox, 2003;Scanes and McNabb, 2003). This has stimulated research on how PCBs affect thyroid function, but most of the research has been done on laboratory mammals.…”