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.

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).

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.