Environmental drivers, including anthropogenic impacts, affect vital rates of organisms. Nevertheless, the influence of these drivers may depend on the physical features of the habitat and how they affect life history strategies depending on individual covariates such as age and sex. Here, the long‐term monitoring (1994–2014) of marked European Shags (Phalacrocorax aristotelis) in eight colonies in two regions with different ecological features, such as foraging habitat, allowed us to test several biological hypotheses about how survival changes by age and sex in each region by means of multi‐event capture–recapture modeling. Impacts included fishing practices and bycatch, invasive introduced carnivores and the severe Prestige oil spill. Adult survival was constant but, unexpectedly, it was different between sexes. This difference was opposite in each region. The impact of the oil spill on survival was important only for adults (especially for females) in one region and lasted a single year. Juvenile survival was time dependent but this variability was not synchronized between regions, suggesting a strong signal of regional environmental variability. Mortality due to bycatch was also different between sex, age and region. Interestingly the results showed that the size of the fishing fleet is not necessarily a good proxy for assessing the impact of bycatch mortality, which may be more dependent on the fishing grounds and the fishing gears employed in each season of the year. Anthropogenic impacts affected survival differently by age and sex, which was expected for a long‐lived organism with sexual size dimorphism. Strikingly, these differences varied depending on the region, indicating that habitat heterogeneity is demographically important to how environmental variability (including anthropogenic impacts) and resilience influence population dynamics.
Martínez-Abraín, A., Oro, D., Velando, A., Genovart, M., Gerique, C., Bartolomé, M.A., Sarzo, B. & Villuendas, E., 2006. Morphometric similarities between central and peripheral populations of the European shag Phalacrocorax aristotelis. Marine Ornithology 34: 21–24.
We compared morphometrics and discriminant functions for sexing European Shags Phalacrocorax aristotelis in a central (British) population and a peripheral (northwestern Iberia) population within its distribution range, to account for structural differences between populations and sexes. Overall, British shags were structurally larger than Iberian shags, except in their head and bill length. This north–south cline could be attributable to higher food availability or lower ambient temperatures at higher latitudes. Furthermore, Iberian male shags were structurally larger than females for all variables considered, except for bill length, which was similar for both sexes, as in the British population. This suggests that bill length is a conservative trait in the species, being similar between populations and sexes alike. The most parsimonious discriminant function for sexing Iberian shags included only bill depth, and it correctly sexed 92.6% of the original cases, as was the case among British shags. This suggests that the depth of the bill likely plays a relevant sex-specific role in the species. Applying discriminant functions derived from one population to other populations can be problematic. However, we found that the bill depth discriminant function for British shags correctly sexed 90.2% of Iberian shags, supporting the idea that, although British shags are larger than northwestern Iberian shags, differences between sexes are of the same magnitude.
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. & 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.
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.
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).