Are immunotoxic effects of lead shot ingestion linked to oxidative stress?

Abstract

The ingestion of lead (Pb) shot used for hunting constitutes the main cause of Pb poisoning in avifauna, but very little is known about the sublethal effects on birds and their consequences at a population level. We studied the relationship between Pb shot ingestion, oxidative stress biomarkers and the immune function in red-legged partridge (Alectoris rufa). Partridges (n=60) were housed in pairs and assigned to three experimental groups: Control (no shot), low dose and high dose. Pb concentration and δ-aminolevulinic acid dehydratase (δ-ALAD) activity, were determined in blood. Malondialdehyde concentration (MDA), total glutathion levels (GSH) and superoxide dismutase activity (SOD) were quantified in red blood cells homogenates. Vitamins (retinol, α-tocopherol) and carotenoid (lutein) levels were analyzed in plasma. Carotenoid-based coloration was studied by digital photographs and beak and eye ring spectrophotometry. Cell-mediated immune and humoral responses were studied using the phytohemagglutinin (PHA)-skin test and the haemagglutination test after antigen injection, respectively. Acute-phase and antibacterial proteins were measured in plasma. Constitutive immune response was tested determining bactericide activity of fresh whole blood. A negative relationship between Pb concentration and δ-ALAD was found. Pb exposure increased levels of GSH and the primary inflammatory response to PHA. In females, δ-ALAD activity was positively correlated with intensitiy of carotenoid-based red coloration and with relative amount of the eye ring area pigmented by carotenoids. GSH concentration was positively associated with blood Pb concentration. Cellular immune response increased with Pb exposure, while humoral immune response decreased. Exposure to Pb in males decreased retinol and lutein levels in plasma. Antioxidant mechanisms appear to be affected by Pb exposure in a different way in females and males. Females may show a hormetic response with the increase of GSH and enhanced cellular immune respose, but at the cost of a loss on carotenoid ornamentation and a reduced humoral immune response. Males exposed to Pb maintained the pigmentation of ornaments and the competence of both immune functions, but showed a more marked decrease of plasma antioxidants. This may reflect a handicap of the carotenoid-antioxidant allocation trade-off in males between the expression of sexual signals and the immunitary response or other oxidative stress-sensitive functions.