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.

Effects of Acute Exposure to Heavy Fuel Oil from the Prestige Spill on a Seabird

Alonso-Alvarez, C., Pérez, C. & Velando, A. Effects of acute exposure to heavy fuel oil from the Prestige spill on a seabird. Aquatic Toxicology 84, 103–110 (2007). doi:10.1016/j.aquatox.2007.06.004.


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

Alonso-Alvarez, C., Munilla, I., López-Alonso, M. & Velando, A. Sublethal toxicity of the Prestige oil spill on yellow-legged gulls. Environment International 33, 773–781 (2007).


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.