In November 2002, the tanker Prestige broke in two and sank at the bottom of the ocean spilling about 70,000 t of fuel oil, which reached the coast of Galicia. It was considered the largest spill in maritime history, greatly affecting marine and related avian species. The spilled fuel oil contained high concentrations of polycyclic aromatic hydrocarbons (PAHs). Many species were affected and were found dead, although ongoing research is still being carried out on the sublethal effects. In this sense, little is known about the action of PAHs on Cholinesterase activity in seabirds. Consequently, the purpose of this study was to provide more information on the neurotoxicity of fuel oil on the seabirds most affected by the Prestige accident: common guillemot, Atlantic puffin and razorbill. On the other hand, data on normal values of acetylcholinesterase (AChE) activity were obtained to supply non-exposed values in seabirds. The oil spill produced a clear inhibitory effect on brain AChE activity in common guillemot (16%, p ≤ 0.01) and razorbill (22%, p ≤ 0.01), but not in Atlantic puffin (4%). Physiological levels of brain AChE, expressed in nmol acetylcholine hydrolysed min− 1 mg− 1 protein were similar in non-exposed common guillemot (388.6 ± 95.0) and Atlantic puffin (474.0 ± 60.7), however, razorbill values were higher (644.6 ± 66.9).
Seabirds are top consumers in marine foodchains which offer opportunities to detect and assess the toxicological effects of different inorganic elements on the marine ecosystem. In order to provide baseline data concerning trace element levels in seabird species from NW Spain, zinc, copper, arsenic, chromium, lead, cadmium and mercury concentrations were analyzed in liver of three different seabird species (common guillemot, Atlantic puffin and razorbill) affected by the Prestige oil spill in September 2002 on the Galician coast. In general, with the exception of mercury, levels of all the analyzed elements were similar or lower in comparison with those reported for the same species in other Atlantic areas, and did not exceed levels indicative of increased environmental exposure.
Velando, A., Munilla, I., López-Alonso, M., Freire, J. & Pérez, C. EROD activity and stable isotopes in seabirds to disentangle marine food web contamination after the Prestige oil spill. Environmental Pollution 158, 1275–1280 (2010).
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.
Velando, A., Munilla, I. & Leyenda, P. M. Short-term indirect effects of the Prestige’ oil spill on European shags: changes in availability of prey. Marine Ecology Progress Series 302, 263–274 (2005).
In 2003, immediately following the ‘Prestige’ oil spill in Galicia, Spain, we studied the reproductive performance of European shags Phalacrocorax aristotelis at Illas Cíes, the main breeding ground for the species in Spain. Over the 10 yr preceding the spill, we monitored the breeding and the dynamics of the Illas Cíes population. We performed 1000 simulations of the population dynamics using the population parameters and their variability for the pre-spill period. The number of breeding
pairs counted in 2003 was lower than any of the values predicted by the simulation models, suggesting that population parameters changed after the ‘Prestige’ wreck. Environmental conditions cannot explain the observed effects because weather conditions were far from severe in 2003. The analysis of shag casualities showed that despite the extensive oiling of Illas Cíes and nearby waters it is unlikely that shags were killed in large numbers. Nevertheless, the shag feeding grounds around Illas Cíes, which are mainly sandy bottoms, were continuously exposed to oil pollution throughout the shag breeding season as revealed by the high levels of pollutants in sediments, plankton, and other organisms. In the pre-spill years, shags showed low seasonal dietary variation, feeding mainly on sandeels. Nevertheless, in 2003, there was a dietary shift with a lower occurrence of sandeel that, together with sandeel fishery data, indicate lower sandeel availability at foraging areas. In addition, reproductive performance in 2003 was significantly lower and chick condition was poorer compared to the pre-spill years. When all this information is taken into account, the picture that emerges strongly suggests that the European Shag population in Illas Cíes is suffering a negative impact of an indirect nature mediated through a reduction on the availability of a highly preferred forage-fish.
Velando, A., Alvarez, D., Mourino, J., Arcos, F. & Barros, A. Population trends and reproductive success of the European shag Phalacrocorax aristotelis on the Iberian Peninsula following the Prestige oil spill. Journal of Ornithology 146, 116–120 (2005).
In 2003, immediately following the Prestige oil spill in Galicia, Spain, we studied the population trends and reproductive performance of European shags (Phalacrocorax aristotelis) at oiled and unoiled colonies. This bird is an important member of the nearshore marine community, breeding in the area affected by the Prestige oil spill. The European shag feeds around the breeding colonies throughout the year, making it a useful indicator of environmental change. Before the oil spill, population trends were similar between oiled and unoiled colonies. Nevertheless, colonies located within the path of the oil suffered greater declines (ca. 10%) compared with pre-spill trends and with population trends at unoiled colonies. In 2003, the breeding success was 50% lower in oiled colonies compared with unoiled colonies. The data available from pre-spill years suggest that the annual reproductive success did not differ among colonies before the impact. European shags breeding at colonies affected by oil showed a negative initial impact from the Prestige oil spill. The reduction in reproductive success at oiled colonies may be due to sublethal effects of oil exposure or low food availability after the oil spill.
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.
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.
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).
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.
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.