Antioxidants safeguard telomeres in bold chicks.

Telomeres are sensitive to damage induced by oxidative stress, and thus it is expected that dietary antioxidants may support the maintenance of telomere length in animals, particularly those with a fast rate of life (e.g. fast metabolism, activity and growth). We tested experimentally the effect of antioxidant supplements on telomere length during early development in wild gull chicks with natural individual variations in behaviour pattern and growth rate. Proactive chicks had shorter telomeres than reactive chicks, but the penalty for the bold behaviour pattern was reduced by antioxidant supplementation. Chicks growing faster had longer telomeres during early growth, suggesting that inherited quality supports a fast life history.

Long-term reproductive impairment in a seabird after the Prestige oil spill.

Large oil spills are dramatic perturbations on marine ecosystems, and seabirds are one of the worst affected organisms in such events. It has been argued that oil spills may have important long-term consequences on marine organisms, but supporting evidence remains scarce. The European shag (Phalacrocorax aristotelis) was strongly impacted at population level by the Prestige oil spill, the biggest spillage in the eastern North Atlantic. In this paper, we report on the long-term consequences on reproduction of this coastal seabird, using temporal and spatial replicated data (before-after-control-impact design). Our study revealed long-term reproductive impairment during at least the first 10 years since the Prestige oil spill. Annual reproductive success did not differ before the impact, but after the impact it was reduced by 45% in oiled colonies compared with unoiled ones. This is a rare documentation of long-term effects after a major oil spill, highlighting the need for long-term monitoring in order to assess the real impact of this type of disturbance on marine organisms.

Oil pollution increases plasma antioxidants but reduces coloration in a seabird.

It has been suggested that condition-dependent signals may be a useful measure of environmental quality. In this study, we tested the hypothesis that oil pollution enhances oxidative stress and impairs expression of a carotenoid-based signal in a wild population of the yellow-legged gull (Larus michahellis). During the courtship period, a group of gulls were fed a supplementary diet containing heavy fuel oil from the Prestige oil spill and were compared with control gulls fed a similar supplementary diet without fuel oil. Blood levels of polycyclic aromatic hydrocarbons, the most toxic components of crude oils, were higher (30%) in the Prestige oil-fed gulls than in the control gulls. Plasma concentrations of vitamin E and carotenoids were also significantly higher in the Prestige oil-fed gulls (31 and 27%, respectively). Although, the plasma levels of lipid peroxidation markers were higher (13%) in gulls fed with Prestige oil than in the control gulls, these differences were not significant, possibly because of the small number of gulls analyzed. The red bill spot was significantly smaller (16%) in the oil-fed gulls than in the control individuals. This study provides the first experimental evidence that a carotenoid-based signal in a free-living seabird is affected by exposure to oil pollution and is hence indicative of environmental quality. Since the yellow-legged gull belongs to a complex of species widely distributed throughout the northern hemisphere, the method described may constitute a useful tool for evaluating sub-lethal effects of oil spills in seabirds.

EROD activity and stable isotopes in seabirds to disentangle marine food web contamination after the Prestige oil spill.

In this study, we measured via surgical sampling hepatic EROD activity in yellow-legged gulls from oiled and unoiled colonies, 17 months after the Prestige oil spill. We also analyzed stable isotope composition in feathers of the biopsied gulls, in an attempt to monitor oil incorporation into marine food web. We found that yellow-legged gulls in oiled colonies were being exposed to remnant oil as shown by hepatic EROD activity levels. EROD activity was related to feeding habits of individual gulls with apparent consequences on delayed lethality. Capture-recapture analysis of biopsied gulls suggests that the surgery technique did not affect gull survival, giving support to this technique as a monitoring tool for oil exposure assessment. Our study highlights the combination of different veterinary, toxicological and ecological methodologies as a useful approach for the monitoring of exposure to remnant oil after a large oil spill.

Sublethal effects on seabirds after the Prestige oil-spill are mirrored in sexual signals.

It has been suggested that sexual signals may be a useful measure of environmental quality as they represent the sum of environmental pressures on the animal. Accordingly, it has been proposed that carotenoid-based coloration may be especially valuable in monitoring and detecting the sublethal effects of toxic pollutants in the environment. Here, we evaluate whether the carotenoid-based coloration in the bill of adult yellow-legged gulls reflects oil-induced sublethal effects in breeding colonies affected by the Prestige oil spill. In 2004, we took blood samples from 27 adult birds at four insular breeding colonies located in the pathway of the Prestige oil spill. We measured the size of the red bill spot area and analysed plasma biochemical parameters indicative of sublethal effects of oil contamination in gulls, including glucose, total protein, creatinine, inorganic phosphorus, aspartate aminotransferase (AST) and gamma-glutamyl transferase. We showed that the size of their red bill spot area was positively related to body condition, while negatively related with AST levels, an enzyme that is commonly used as an indication of hepatic damage in birds. Hence, the present study provides support for the idea that carotenoid-based colour integuments may be a useful measure of environmental quality.

Monitoring polycyclic aromatic hydrocarbon pollution in the marine environment after the Prestige oil spill by means of seabird blood analysis.

In this study we tested the use of seabird blood as a bioindicator of polycyclic aromatic hydrocarbon (PAH) pollution in the marine environment. Blood cells of breeding yellow-legged gulls (Larus michahellis) were able to track spatial and temporal changes consistent with the massive oil pollution pulse that resulted from the Prestige oil spill. Thus, in 2004, blood samples from yellow-legged gulls breeding in colonies that were in the trajectory of the spill doubled in theirtotal PAH concentrations when compared to samples from unoiled colonies. Furthermore, PAH levels in gulls from an oiled colony decreased by nearly a third in two consecutive breeding seasons (2004 and 2005). Experimental evidence was gathered by means of an oil-ingestion field experiment. The total concentration of PAHs in the blood of gulls given oil supplements was 30% higher compared to controls. This strongly suggested that measures of PAHs in the blood of gulls are sensitive to the ingestion of small quantities of oil. Our study provides evidence that seabirds were exposed to residual Prestige oil 17 months after the spill commenced and gives support to the nondestructive use of seabirds as biomonitors of oil pollution in marine environments.

Effects of acute exposure to heavy fuel oil from the Prestige spill on a seabird.

Large quantities of petroleum products are released into the marine environment as result of tanker wrecks. Such catastrophic events have a dramatic impact on marine ecosystems, affecting a broad range of species. Seabirds are placed at the uppermost trophic level of the marine food chain. Therefore, important toxic effects are expected in these organisms. The recent Prestige oil spill gave the opportunity to test this. A previous study reported that yellow-legged gulls (Larus michahellis) breeding in the oiled area (17 months after the spill) showed differences both in plasma biochemistry and in the total circulating levels of polycyclic aromatic hydrocarbons (TPAHs) in blood regard to gulls sampled in clean areas. In the present study, wild yellow-legged gulls were fed with heavy fuel oil from the Prestige oil spill (P-gulls) and compared with control gulls (C-gulls) fed only with the vehicle (vegetable oil). Consistent with the cited previous findings, gulls fed with fuel oil showed reduced glucose and inorganic phosphorus levels in plasma, as well as a trend to significantly reduced creatinine values. In addition, glucose concentration was negatively related to TPAH levels. Males but not females fed with fuel oil showed higher plasma activity of asparatate aminotransferase (AST) than controls. With regard to plasma activity of gamma-glutamyl transferase (GGT), the results were opposite to the previous study. The GGT activity increased in C-females, apparently to meet with increased liver metabolism due to egg laying demands, but not in P-females. Differences to the previous study possibly reflect different adaptive responses of these enzymes to an acute short-term exposure to heavy fuel oil. Since the yellow-legged gull belongs to a complex of species widely distributed throughout the Northern hemisphere, the results as a whole might provide a tool for future evaluations of short- and long-term effects of oil spills on seabirds. Decreased glucose and inorganic phosphorus levels in plasma are expected in both short- and long-lasting exposures to fuel oil, whereas responses of AST and GGT enzymes would depend on both the sex of individuals and the temporal pattern of exposure.

Sublethal toxicity of the Prestige oil spill on yellow-legged gulls.

The Prestige oil spill in November 2002 is considered the biggest large-scale catastrophe of its type in Europe, thousands of seabirds dying in the subsequent months. Here, the total concentration of 16 polycyclic aromatic hydrocarbons (TPAH) was measured in the blood cell fraction of adult and chick yellow-legged gulls (Larus michahellis) from unoiled and oiled coastal areas in North Western Spain. In addition, hematocrit, plasma metabolites, electrolytes and enzymes, as well as body mass were determined in the same individuals. Our results strongly suggest the presence of health damages of sublethal nature in adult gulls breeding in oiled colonies 17 months after the Prestige oil spill. This is supported by the following evidences: (1) gulls sampled in unoiled and oiled colonies differed in blood TPAH levels, (2) gulls sampled in unoiled and oiled colonies differed in several blood parameters indicative of physiological disorders, and (3) TPAH in blood was significantly related to several of these parameters. Differences in the level of asparatate aminotransferase (AST), gamma-glutamyl transferase (GGT), total protein, glucose and inorganic phosphorus suggest damages on some vital organs (i.e. liver and kidney) in adult birds from oiled areas. Meanwhile, chicks presented weaker effects than adults, showing only between-area differences in hematocrit. Since TPAH levels in blood did not differ between both age-groups, the stronger effects on adults should be due to their longer exposure to these pollutants and/or to severe exposure in the months following the spill. The presence of PAHs in chicks indicates that these pollutants were incorporated into the food chain because nestlings would have been only exposed to contaminated organisms in the diet (e.g. fishes and crustaceans). Our findings support the view that PAHs may deeply alter the physiology of seabirds, and emphasize the necessity of quantifying the circulating levels of these compounds in order to evaluate the sublethal effects associated to large oil spills.