Assessing the effects of the Prestige oil spill on the European shag (Phalacrocorax aristotelis): trace elements and stable isotopes

Sanpera, C., Valladares, S., Moreno, R., Ruiz, X. & Jover, L. Assessing the effects of the Prestige oil spill on the European shag (Phalacrocorax aristotelis): trace elements and stable isotopes. Science of the total environment 407, 242–249 (2008).


The Prestige oil spill resulted in the mortality of several seabird species on the Atlantic NW coast of Spain. Shag casualties were particularly relevant, since populations are resident in the area the whole year round and because of several features which make them highly vulnerable to environmental hazards. Ecological catastrophes give us the opportunity of collecting samples which, otherwise, would be difficult to obtain. We examine the potential of shag corpses as bioindicators of inorganic pollution and the possible factors of variability, such as biological traits (sex, age) or nutrition status. We determined trace elements (Hg, Se, Cr, Pb, Zn and Cu) and isotopic signatures (15N, 13C) in soft tissues (muscle, liver) and in primary feathers formed at different times (before and after the Prestige) in individuals of known sex and age, collected at the time of the Prestige disaster. These were compared with data from another group of shags trapped accidentally in fishing gear in 2005. Our results did not seem to be affected by sex or age on any of the analysed variables. The higher nitrogen isotopic signatures in  the soft tissues of the Prestige shags may be related to the nutrition stress caused by a poorer body condition,which is also reflected in increasing levels of some metals in the liver.This isotopic enrichment was also observed in newly forming feathers when compared to the old ones. On the other hand, the lower δ15N and Hg values in shag feathers from2005 point to a shift in feeding resources to prey of lower trophic levels.We found that feather features (being an inert tissue and having a conservative composition), if combined with careful dating and chemical analysis, offer a very useful tool to evaluate temporal and spatial changes in seabird ecology in relation to pollution events.

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

Pérez, C., Velando, A., Munilla, I., López-Alonso, M. & Oro, D. Monitoring Polycyclic Aromatic Hydrocarbon Pollution in the marine environment after the Prestige oil spill by means of seabird blood analysis. Environmental Science & Technology 42, 707–713 (2008).


In this studywetested 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 their total 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.

Oil pollution increases plasma antioxidants but reduces coloration in a seabird

Pérez, C., Lores, M. & Velando, A. Oil pollution increases plasma antioxidants but reduces coloration in a seabird. Oecologia 163, 875–884 (2010).


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 yellowlegged 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 freeliving 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 sublethal effects of oil spills in seabirds.

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

Perez, C., Munilla, I., Lopez-Alonso, M. & Velando, A. Sublethal effects on seabirds after the Prestige oil-spill are mirrored in sexual signals. Biology Letters 6, 33–35 (2010).


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.

Oiling of live gulls as a tool to monitor acute oil spill effects on seabirds

Munilla, I. & Velando, A. Oiling of live gulls as a tool to monitor acute oil spill effects on seabirds. Ibis 152, 405–409 (2010).


Here we present a novel non-intrusive approach that can be useful to assess oil effects on seabirds based on the monitoring of oiling rates in live free-ranging gulls. To assess the feasibility of this method, we established a monitoring scheme to record oiling rates in live gulls in a coastal area affected by the Prestige oil spill disaster in Galicia (northwest Spain).

Seabird feathers as monitors of the levels and persistence of heavy metal pollution after the Prestige oil spill

Moreno, R., Jover, L., Diez, C. & Sanpera, C. Seabird feathers as monitors of the levels and persistence of heavy metal pollution after the Prestige oil spill. Environmental pollution 159, 2454–2460 (2011).


We measured heavy metal concentrations in yellow-legged gulls (n=196) and European shags (n=189) in order to assess the temporal pattern of contaminant exposure following the Prestige oil spill in November 2002. We analysed Pb, Cu, Zn, Cr, Ni and V levels in chick feathers sampled at four colonies during seven post-spill years (2003-2009), and compared results with pre-spill levels obtained from feathers of juvenile shag corpses (grown in spring/summer 2002). Following the Prestige wreck, Cu (4.3-10 mg g-1) and Pb concentrations (1.0e1.4 mg g-1) were, respectively, between two and five times higher than prespill
levels (1.5-3.6 and 0.1-0.4 mg g-1), but returned to previous background concentrations after three years. Our study highlights the suitability of chick feathers of seabirds for assessing the impact of oil spills on heavy metal contamination, and provides the best evidence to date on the persistence of oil pollution after the Prestige incident.

Ten Years after the Prestige Oil Spill: Seabird Trophic Ecology as Indicator of Long-Term Effects on the Coastal Marine Ecosystem

Moreno, R., Jover, L., Diez, C., Sardá, F. & Sanpera, C. Ten Years after the Prestige Oil Spill: Seabird Trophic Ecology as Indicator of Long-Term Effects on the Coastal Marine Ecosystem. PLoS ONE 8, e77360 (2013).


Major oil spills can have long-term impacts since oil pollution does not only result in acute mortality of marine organisms, but also affects productivity levels, predator-prey dynamics, and damages habitats that support marine communities. However, despite the conservation implications of oil accidents, the monitoring and assessment of its lasting impacts still remains a difficult and daunting task. Here, we used European shags to evaluate the overall, lasting effects of the Prestige oil spill (2002) on the affected marine ecosystem. Using δ15N and Hg analysis, we trace temporal changes in feeding ecology potentially related to alterations of the food web due to the spill. Using climatic and oceanic data, we also investigate the influence of North Atlantic Oscillation (NAO) index, the sea surface temperature (SST) and the chlorophyll a (Chl a) on the observed changes. Analysis of δ15N and Hg concentrations revealed that after the Prestige oil spill, shag chicks abruptly switched their trophic level from a diet based on a high percentage of demersal-benthic fish to a higher proportion of pelagic/semi-pelagic species. There was no evidence that Chl a, SST and NAO reflected any particular changes or severity in environmental conditions for any year or season that may explain the sudden change observed in trophic level. Thus, this study highlighted an impact on the marine food web for at least three years. Our results provide the best evidence to date of the long-term consequences of the Prestige oil spill. They also show how, regardless of wider oceanographic variability, lasting impacts on predator-prey dynamics can be assessed using biochemical markers. This is particularly useful if larger scale and longer term monitoring of all trophic levels is unfeasible due to limited funding or high ecosystem complexity.