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.

Differential effects of specific carotenoids on oxidative damage and immune response of gull chicks

Lucas, A., Morales, J. & Velando, A. Differential effects of specific carotenoids on oxidative damage and immune response of gull chicks. Journal of Experimental Biology 217, 1253–1262 (2014).


Micronutrients are essential for normal metabolic processes during early development. Specifically, it has been suggested that diet-derived carotenoids can play a key role in physiological functions because of their antioxidant and immunostimulant properties. However, their role as antioxidants remains controversial. Additionally, it is also unclear whether oxidative stress mediates their immunostimulatory effects. In this field study, we separately supplemented yellow-legged gull (Larus michahellis) chicks with two carotenoids (lutein and β-carotene) with different molecular structures and different transformation pathways into other oxidative forms of carotenoids. We quantified their effect on the oxidative status and the immune response of chicks before and after an oxidative challenge with paraquat, a pro-oxidant molecule. Prior to oxidative challenge, none of the carotenoid treatments affected the oxidative status of chicks, but they enhanced the inflammatory response to an antigen compared with controls. The oxidative challenge enhanced plasma vitamin E levels (but not in β-carotene-supplemented chicks) and the antioxidant capacity in the short term. Interestingly, lutein-supplemented chicks showed lower oxidative damage to proteins than non-lutein-supplemented chicks. After the oxidative challenge, the positive effect of carotenoid supplementation on the immune response disappeared. Thus, these results suggest differential effects of two carotenoids with different molecular structures on the oxidative status. Lutein but not β-carotene helps to combat oxidative damage after a free-radical exposure. Additionally, the results indicate that the immunostimulatory effects of carotenoids are linked to oxidative status during early life.

Invasiones biológicas en islas: dinámicas, impactos y gestión

Latorre Piñeiro, L. Invasiones biológicas en islas: dinámicas, impactos y gestión. (Universidade de Santiago de Compostela, 2013).


• Todos los mamíferos invasores estudiados ejercieron impactos negativos de distinto grado sobre la fauna y/o flora de las islas que los hospedan. La rata negra afectó tanto a plantas nativas, reduciendo la supervivencia de semillas, como a comunidades de aves marinas, depredando sus huevos. El conejo europeo mostró un efecto sobre plantas nativas en dos islas, afectando al menos a dos especies vegetales (Medicago citrina y Armeria pubigera), reduciendo la supervivencia de las plántulas de una y el crecimiento vegetativo de la otra. El análisis de la dieta de gato asilvestrado y visón americano indicó efectos de moderados a
fuertes sobre aves marinas, además de efectos potenciales sobre otros animales nativos.
• Al aumentar el número de especies invasoras de los sistemas estudiados, aparecieron efectos combinados, sinérgicos e indirectos sobre la biota nativa. Los complejos de invasión están asociados con dinámicas ecológicas complejas como la hiperdepredación y la liberación del mesodepredador, con sus consecuencias potenciales sobre la biota nativa.
• Los datos y simulaciones presentadas fueron utilizados para evaluar la viabilidad de estrategias alternativas al control o erradicación de especies invasoras. Por ejemplo, la reintroducción de especies vegetales protegidas en islas se puede complementar con una protección específica frente a herbívoros invasores; haciendo especial hincapié en las fases del ciclo vital de la planta más vulnerables. Otro ejemplo de posible estrategia alternativa de gestión tratada en el presente trabajo
es el uso de aversivos químicos (aversión condicionada al sabor) para proteger los nidos de aves marinas de la depredación por rata negra. Las especies de huevos con menor tamaño deberían tener prioridad ya que sus huevos son más vulnerables a la depredación.
• Los estudios de las especies invasoras y sus impactos son imprescindibles para determinar la efectividad de los métodos alternativos de control. Estos estudios deben ser más exhaustivos cuanto más amplio sea el complejo de invasión a tratar. Se comprobó que el uso de modelos computacionales simples que incorporan las relaciones tróficas entre especies invasoras y nativas, son altamente útiles para este propósito. Por lo menos uno de los modelos testados reveló ser especialmente sensible a ciertos parámetros, como la tasa de crecimiento de todas las especies implicadas, las tasas de depredación y la preferencia de presas por parte del depredador y la capacidad de carga específica de una de las presas. Se debe prestar especial atención a la recolección de estos parámetros en campo para obtener estimas fiables, tanto para realizar simulaciones como para el monitoreo del plan de manejo finalmente elegido.
• Los resultados expuestos en la presente tesis sugieren que los proyectos de manejo de complejos de invasión son empresas exigentes que requieren tanto inversiones adecuadas (necesarias para asegurar altos niveles de eficiencia en el control, en nuestro caso > 70%) como esfuerzos prolongados (en nuestro caso, de 8 a 10 años en la simulación más optimista para Sálvora, y control permanente en las Cíes para prevenir el declive de las colonias de aves marinas). Tales niveles de financiación y duración son mucho más de lo que hoy en día se aplica en España. La ejecución de programas de control insuficientes, discontinuos o esporádicos se deben evitar, no solo por la pérdida de tiempo y dinero que supone, sino porque puede llevar a efectos no deseados, como el desarrollo de resistencia fisiológica a venenos o la evasión aprendida de trampas en el caso de las especies invasoras, o incluso tasas de depredación inusualmente altas de biota nativa, durante picos poblacionales de especies invasoras tras el cese temprano de programas de control.

Antioxidants safeguard telomeres in bold chicks

Kim, S.-Y. & Velando, A. Antioxidants safeguard telomeres in bold chicks. Biology letters 11, 20150211 (2015).


Telomeres are sensitive to damage induced by oxidative stress, and thus it is expected that dietary antioxidants may support the maintenance of telomere length in animals, particularly those with a fast rate of life (e.g. fast metabolism, activity and growth). We tested experimentally the effect of antioxidant supplements on telomere length during early development in wild gull chicks with natural individual variations in behaviour pattern and growth rate. Proactive chicks had shorter telomeres than reactive chicks, but the penalty for the bold behaviour pattern was reduced by antioxidant supplementation. Chicks growing faster had longer telomeres during early growth, suggesting that inherited quality supports a fast life history.

Spatial patterns of seed dispersal and seedling recruitment in Corema album (Empetraceae): the importance of unspecialized dispersers for regeneration

Calviño-Cancela, M. Spatial patterns of seed dispersal and seedling recruitment in Corema album (Empetraceae): the importance of unspecialized dispersers for regeneration. Journal of Ecology 90, 775–784 (2002). DOI: 10.1046/j.1365-2745.2002.00711.x


  • Spatial patterns of seed dispersal and seedling recruitment of Corema album were examined among and within habitats to determine the quantitative importance of different dispersers in each type of habitat, and their effectiveness in carrying seeds to suitable habitats for seedling recruitment.
  • Gulls, blackbirds and rabbits were, respectively, the main dispersers (45%, 40% and 15% of Corema album seeds). Within habitats, blackbirds disperse seeds mainly to female Corema album shrubs, while gulls and rabbits disperse seeds mainly to open ground.
  • The quantitative role of dispersers varies among habitats because of their habitat preferences, causing the spatial pattern of seed rain to differ.
  • Open ground has the highest density of seedlings and the highest seedling-to-seed ratios. Regeneration is more active in the pioneer scrub than in the mature scrub and the herbaceous vegetation.
  • Gulls, rather than specialist frugivores, are the most effective dispersers in carrying seeds to suitable sites for recruitment.

Effectiveness of a varied assemblage of seed dispersers of a fleshy-fruited plant

Calviño-Cancela, M. & Martín-Herrero, J. Effectiveness of a varied assemblage of seed dispersers of a fleshy-fruited plant. Ecology 90, 3503–3515 (2009).


Disperser effectiveness is the number of new plants resulting from the activity of one disperser relative to other dispersers or to nondispersed seeds. Effectiveness remains largely uninvestigated due to the complexity of its measurement. We measured the effectiveness of seed dispersers (Larus michahellis, Turdus merula, and Oryctolagus cuniculus) of the shrub Corema album (Empetraceae) using a simulation model of the recruitment process that was parameterized with field data of seed dispersal, predation, and seedling emergence and validated with independent data on seedling density. The model allows tracking the fate of seeds dispersed by each animal and estimating, for the first time, disperser effectiveness as seedlings per square meter contributed by each disperser. It also allows quantifying the relative importance of different recruitment processes in determining the quantity and spatial distribution of recruitment. Larus michahellis was the most effective disperser in two of the three habitats studied,contributing 3–125 times more than the other two species, whose lower effectiveness depended
mostly on deposition patterns (T. merula) or deleterious effects on seedling emergence (O.cuniculus). The dependence of the plant on each disperser differed between habitats and was the greatest in sparse scrub, where recruitment depended almost exclusively on gulls (90%). Quantity and quality of dispersal were not correlated; quality was a better predictor of disperser effectiveness. Seedling emergence was the most crucial process in determining both the spatial pattern of recruitment among microhabitats (99.8% of variance explained) and the quantity of recruitment within microhabitats (43–83%). A sensitivity analysis showed that increasing seed dispersal improved the recruitment for all dispersers when there was no competition for fruits. However, with limited fruits, increased dispersal of lower quality dispersers reduced overall recruitment. Our results show important differences in effectiveness among dispersers and illustrate the different influences of the components of effectiveness, which varied depending not only on the disperser but also on the circumstances (e.g., type of habitat).

Female body condition and brood sex ratio in yellow-legged gulls Larus cachinnans

Alonso-Alvarez, C. & Velando, A. Female body condition and brood sex ratio in yellow-legged gulls Larus cachinnans. Ibis 145, 220–226 (2003).


In the Yellow-legged Gull (Larus cachinnans), males are the larger sex, and show more reproductive variance than females. We predicted that the proportion of male chicks in a brood should increase with female body condition. We investigated brood sex ratio by using DNA markers taken from samples of hatchlings or dead embryos, and female body condition using plasma cholesterol concentration as a reliable indicator. The brood sex ratio of females in good condition was male biased and the sex ratio of females in poor condition was female biased. This relationship was also significant in those nests where all the eggs laid were sexed. Thus, manipulation of embryo mortality cannot explain the biases reported in this study, suggesting that the sex ratio of the eggs was biased prior to laying. These results confirm that sex-ratio manipulation in gulls operates under natural conditions, and supports earlier experimental findings.

Changes in plasma biochemistry and body mass during incubation in the yellow-legged gull

Alonso-Alvarez, C., Velando, A., Ferrer, M. & Veira, J. A. Changes in plasma biochemistry and body mass during incubation in the yellow-legged gull. Waterbirds 25, 253–258 (2002).


The “Incubatory Reserves Constancy” hypothesis asserts that incubation could be a departure from breeding stress that allows for the maintenance or recovery of body reserves after laying effort (females) or territory defense (males) in those species with bi-parental incubation such as gulls. The plasma composition and body mass of incubating Yellow-legged Gulls (Larus cachinnans) were analyzed and related to the number of days after egg-laying. Female gulls showed an increase in uric acid and cholesterol levels, whereas males showed only an increase in uric acid values throughout this period. Moreover, females increased while males maintained their body masses. These results could reflect a recovery process after the laying effort supporting the Incubatory Reserves Constancy hypothesis in females. Uric acid and urea levels are positively correlated to body condition in Yellow-legged Gulls, which could be the result of a change in diet composition. This disagrees with recent findings on body composition in incubating gulls and could be related to variations in food availability among populations or years, and could reflect flexibility in the investment devoted by each sex.

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.