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.

Sex-specific mortality of European shags after the Prestige oil spill: demographic implications for the recovery of colonies

Martínez-Abraín, A. et al. Sex-specific mortality of European shags after the Prestige oil spill: demographic implications for the recovery of colonies. Marine Ecology – Progress Series 318, 271–276 (2006).

Oil spills are extreme environmental perturbations (i.e. ecological catastrophes) affecting marine food webs and especially top predators, in which effects are likely amplified. As such, seabirds suffer from direct mortality and food depletion, with potentially important consequences for the population growth rate and probability of extinction. However, little is known about the effects of sex-skewed mortality (due to sex spatio-temporal differences in at-sea distribution) in seabird population
dynamics. We analyzed the mortality of European shags Phalacrocorax aristotelis after the Prestige oil spill and its effects on breeding colonies in Galicia (southwest North Atlantic). Most adults found dead were females (85%). The year after the spill, Monte Carlo simulations of population trajectories predicted a reduction of 11% in the number of breeding pairs when skewed mortality was considered, and a lower rate (8%) when assuming random sex distribution of adult mortality. The further reduction predicted with the sex-biased mortality was probably the result of unmated adults unable to reproduce. This difference, although slight, is a concern for conservation owing that the colonies studied were already showing a 5% annual decline due to other factors also related to human activities.

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

Barros, Á., Álvarez, D. & Velando, A. Long-term reproductive impairment in a seabird after the Prestige oil spill. Biology letters 10, 20131041 (2014).

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.

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.

Mass mortality of seabirds in the aftermath of the Prestige oil spill

Munilla, Ignacio, José Manuel Arcos, Daniel Oro, David Álvarez, Patricia M. Leyenda & Alberto Velando. “Mass mortality of seabirds in the aftermath of the Prestige oil spill.” Ecosphere 2, no. 7 (2011): 1-14.

In the winter of 2002–03 the Prestige tanker spilled 60,000 tons of oil over the northern half of the Iberian Coastal Large Marine Ecosystem (northern Portugal to France). Most (c. 85%) of the 22,981 oiled seabirds reported were alcids (i.e., auks): Common Murres (Uria aalge), Razorbills (Alca torda) and Atlantic Puffins (Fratercula arctica). Here we estimated the mortality of alcids in Galicia (northwestern Spain), the area that received most of the Prestige oil and where half of the oiled seabirds were collected. We performed three experiments that included: (1) a test of several drift block models in open sea, to select the one that best fitted the drift of alcid carcasses; (2) the release of 450 drift blocks at 9 offshore points to assess the recovery rate of oiled alcids and its spatial variation; (3) the assessment of beach survey effort and the detectability of drift blocks. Mean mortality estimates and their bootstrapped confidence intervals were obtained through an estimation model that established: (1) a temporal limit of 23 days to block drifting; (2) spatial differences in the recovery rates of blocks depending on how far away from the coast they were released; (3) a correction factor accounting for detectability, and (4) the distribution pattern of the three alcid species involved according to three distance classes, based on ship surveys. The Prestige oil spill, in terms of acute seabird mortality, was one of the worst oil spills ever reported worldwide. Compared to other major oil spills the estimated mortality for the Prestige oil spill was higher than expected from the number of carcasses retrieved. We recommend that drift block assessments of seabird mortality should be included in contingency response plans to oil pollution emergencies; therefore, a supply of drift-blocks designed to mimic the drifting behavior of the marine bird species of interests should be at hand.