Adrenocortical Response to Stress and Thyroid Hormone Status in Free-Living Nestling White Storks (Ciconia Ciconia) Exposed to Heavy Metal and Arsenic Contamination
Baos, Raquel, Blas, Julio, Bortolotti, Gary R., Marchant, Tracy A., Hiraldo, Fernando, Environmental Health Perspectives
BACKGROUND/OBJECTIVE: Endocrine parameters have proven useful in the detection of early or low-level responses to pollutants. Although most of the studies on endocrine modulation have been focused on processes involving gonadal steroids, contaminants may target other parts of the endocrine system as well. In this study we examined the adrenocortical stress response and thyroid hormone status in free-living nestling white storks (Ciconia ciconia) in relation to heavy metals (zinc, lead, copper, cadmium) and arsenic levels in blood.
METHODS: Fieldwork was conducted in an area polluted by the Aznalcollar mine accident (southwestern Spain) and in a reference site. We used a standardized capture, handling, and restraint protocol to determine both baseline and maximum plasma corticosterone. Circulating levels of thyroxine ([T.sub.4]) and triiodothyronine ([T.sub.3]) were also measured.
RESULTS: No effects of metals or As were found on baseline corticosterone, but maximum levels of corticosterone were positively related to Pb in both locations. This relationship was stronger in single nestlings than in birds from multiple-chick broods, which suggests a greater impact of Pb on more stressed individuals. Metal pollution did not affect plasma [T.sub.4] or [T.sub.3] levels, although thyroid status differed with location.
CONCLUSIONS: Because a compromised hypothalamus-pituitary-adrenal (HPA) function can have far-reaching consequences in terms of altered behavioral and metabolic processes necessary for survival, our results suggest that birds exposed to sublethal Pb levels may be at risk through an altered adrenocortical stress response, and further support the idea that HPA axis-related end points might be useful indicators of metal exposure and potential toxicity in wild animals.
KEY WORDS: Aznalcollar, corticosterone, free-living birds, handling-restraint protocol, lead, metal pollution, stress response, thyroxine, triiodothyronine, white stork. Environ Health Perspect 114:1497-1501 (2006). doi:10.1289/ehp.9099 available via http://dx.doi.org/ [Online 11 July 2006]
In nature, animals can be used as bioindicators to provide an early warning of potential adverse, contaminant-related effects on organisms or populations themselves, on organisms or populations that prey upon them, and as sentinels for exposure and effects on humans (Fox 2001).
Endocrine assessment is a useful diagnostic tool in the detection of early or low-level responses to pollutants, responses that may precede more significant health problems (Kendall et al. 1998). Although most of the studies on endocrine disruption or modulation have been focused on reproductive problems and behavioral abnormalities related to reproduction, contaminants may target other parts of the endocrine system more commonly than they disrupt processes involving gonadal steroids (Damstra et al. 2002; Hinson and Raven 2006). The hypothalamus-pituitary-adrenal (HPA) axis is an important system that regulates and integrates many physiologic functions in response to environmental stressors (Wingfield and Kitaysky 2002). Activation of the HPA axis during a stress response results in glucocorticoid secretion from the adrenal glands (mainly corticosterone in birds). This, in turn, initiates several important physiologic changes including effects on intermediary metabolism, growth, immune function, and inflammatory responses (reviewed by Kitaysky et al. 2003; Sapolsky et al. 2000). Thyroid hormones--thyroxine ([T.sub.4]) and triiodothyronine ([T.sub.3])--also play an important role in metabolism and exert profound effects on avian development (both differentiation and growth) (McNabb 2000).
The impairment of adrenal or thyroid function by contaminant exposure may occur in the absence of gross toxicologic effects and may be critical to developing individuals, with severe consequences such as reduced growth, reduced cognitive capabilities, and impaired immune function (Schantz and Widholm 2001; Smits et al. …