Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird

Kim, S.Y., Noguera, J.C., Morales, J. & Velando, A., 2011. Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird. Evolutionary ecology, 25(2), pp.461-472.


Why do animals not grow at their maximal rates? It has been recently proposed that fast growth leads to the accumulation of cellular damages due to oxidative stress, influencing subsequent performances and life span. Therefore, the trade-off between fast growth and oxidative stress may potentially function as an important constraint in the evolution of growth trajectories. We test this by examining a potential antagonistic pleiotropy between growth and blood resistance to controlled free radical attack in a wild bird using a cross-fostering design and robust quantitative genetic analyses. In the yellow-legged gull Larus michahellis decreased resistance to oxidative stress at age 8 days was associated with faster growth in mass, across the first 8 days of life, suggesting a trade-off between mass growth and oxidative-stress-related somatic maintenance. We found a negative genetic correlation between chick growth and resistance to oxidative stress, supporting the presence of the genetic trade-off between the two traits. Therefore, investment of somatic resources in growth could be constrained by resistance to oxidative stress in phenotypic and genetic levels. Our results provide first evidence for a potential genetic trade-off between life-history and underlying physiological traits in a wild vertebrate. Future studies should explore genetic trade-offs between life-history traits and other oxidative-stress-related traits.

Heritability of resistance to oxidative stress in early life

Kim, S.Y., Noguera, J.C., Morales, J. & Velando, A., 2010. Heritability of resistance to oxidative stress in early life. Journal of Evolutionary Biology, 23(4), pp.769-775.


Oxidative stress has recently been suggested to play an important role in life-history evolution, but little is known about natural variation and heritability of this physiological trait. Here, we explore phenotypic variation in resistance to oxidative stress of cross-fostered yellow-legged gull (Larus cachinnans) chicks. Resistance to oxidative stress was not related to plasma antioxidants at hatching, which are mostly derived from maternal investment into eggs. Common environmental effects on phenotypic variation in resistance to oxidative stress were not significant. Heritability was relatively low and nonsignificant in hatchlings, but interestingly, the chicks of age 8 days showed high and significant heritability (h2 = 0.59). Our results suggest that resistance to oxidative stress is determined mainly by the genotype as chicks grow. Further work is required to explore the genetic role of oxidative stress in life-history evolution.

Morphometric similarities between central and peripheral populations of the European shag Phalacrocorax aristotelis

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.

Sandwich terns Sterna sandvicensis feeding juveniles during autumn migration around the NW Iberian Peninsula

Fernandez-Cordeiro, A. and Costas, R., 1991. Sandwich terns Sterna sandvicensis feeding juveniles during autumn migration around the NW Iberian Peninsula. Seabird, 13, pp.70-71.


The Sandwich Tern Sterna sandvicensis is the tern most frequently observed off the Iberian Atlantic coast, being especially abundant in the Rias Bajas of Galicia (NW Iberian Peninsula), where it winters regularly in small numbers (about 260 individuals; Berrnejo et al. 1985, 1986). The Rias Bajas are the northern edge of the regular winter range in the Iberian Peninsula (Fernandez-Cordeiro & Costas in press).

Thrifty development: early‐life diet restriction reduces oxidative damage during later growth

Noguera, J.C., Lores, M., Alonso‐Álvarez, C. and Velando, A., 2011. Thrifty development: early‐life diet restriction reduces oxidative damage during later growth. Functional Ecology, 25(5), pp.1144-1153.


1. Conditions during early stages of life may have an important effect on phenotype, by inducing programmed responses that may remain throughout the lifetime of an animal. One very important factor that can promote long-term changes in phenotype is restriction of food intake (dietary restriction, DR).
2. Recently, it has been shown that DR may induce an increase in antioxidant and repair mechanisms as a result of hormetic responses. Interestingly, the induction of antioxidant and repair mechanisms may be triggered by transitory increases in reactive oxygen species. Dietary-derived antioxidants, such as vitamin E, may be important to determine the compensatory effect of DR.
3. To investigate the effect of DR on attenuation of oxidative damage, we manipulated dietary intake (by restricting food ingestion) and antioxidant availability (by vitamin E supplementation) during the first days of life of yellow-legged gull (Larus michahellis) chicks. We then measured oxidative status and body mass during the early development of chicks.
4. We found that an early short event of food shortage strongly affected the oxidative status of the chicks and their growth patterns. We observed less oxidative damage to proteins and DNA in dietary restricted chicks, after the period of food restriction, than in non-restricted chicks. Unexpectedly, vitamin E supplementation did not suppress the hormetic effect of DR, but instead increased it.
5. These novel results support the idea that short events of DR during early development induce a reduction in oxidative damage in wild animals. The results suggest that DR promotes the induction of an early hormetic response in some antioxidant defence processes and/or repair mechanisms. These findings have important implications for our understanding of how early conditions may shape the phenotype of an organism, and also for the study of evolutionary trade-offs during early growth.

Toxoplasma gondii infection in seagull chicks is related to the consumption of freshwater food resources

Cabezón, O., Cerdà-Cuéllar, M., Morera, V., García-Bocanegra, I., González-Solís, J., Napp, S., Ribas, M.P., Blanch-Lázaro, B., Fernández-Aguilar, X., Antilles, N. & López-Soria, S., 2016. Toxoplasma gondii Infection in Seagull Chicks Is Related to the Consumption of Freshwater Food Resources. PloS one, 11(3), p.e0150249.

Understanding the spread of Toxoplasma gondii (T. gondii) in wild birds, particularly in those with opportunistic feeding behavior, is of interest for elucidating the epidemiological involvement of these birds in the maintenance and dissemination of the parasite. Overall, from 2009 to 2011, we collected sera from 525 seagull chicks (Yellow-legged gull (Larus michahellis) and Audouin’s gull (L. audouinii)) from 6 breeding colonies in Spain and tested them using the modified agglutination test (MAT) for the presence of antibodies against T. gondii. Chick age was estimated from bill length. Main food source of seagull chicks was evaluated using stable isotope analyses from growing scapular feathers. Overall T. gondii seroprevalence was 21.0% (IC95% 17.5–24.4). A generalized linear mixed-effects model indicated that year (2009) and food source (freshwater) were risk factors associated to the individual risk of infection by T. gondii, while age (days) was close to significance. Freshwater food origin was related to the highest seroprevalence levels, followed by marine origin, supporting freshwater and sewages as important routes of dispersion of T. gondii. Year differences could indicate fluctuating rates of exposure of seagull chicks to T. gondii. Age ranged from 4 to 30 days and seropositivity tended to increase with age (P = 0.07), supporting that seropositivity is related to T. gondii infection rather than to maternal transfer of antibodies, which in gulls is known to sharply decrease with chick age. This study is the first to report T. gondii antibodies in Yellow-legged and Audouin’s gulls, thereby extending the range of intermediate hosts for this parasite and underscoring the complexity of its epidemiology.

The importance of hatching date for dominance in young shags

Velando, A., 2000. The importance of hatching date for dominance in young shags. Animal Behaviour, 60(2), pp.181-185.


In birds, conditions and experience in the nest may influence the social rank of juveniles after they become independent. Three main factors may be involved: (1) mass at fledging, larger birds being better able to compete; (2) brood hierarchy, dominance in the brood continuing after the birds leave the nest; and (3) hatching date, birds hatching earlier having more experience and a greater ability to compete. I studied the effect of these factors on the agonistic behaviour of juvenile European shags, Phalacrocorax aristotelis, in crèches. Of all the factors, only hatching date had a significant influence on the dominance rank of juveniles. Birds that hatched earlier had a higher rank. Additionally, males were somewhat more aggressive than females. The importance of an individual’s hatching date for its social rank may have consequences for its future reproductive value.

Acetylcholinesterase activity in seabirds affected by the Prestige oil spill on the Galician coast (NW Spain)

Oropesa, A.L., Pérez-López, M., Hernández, D., García, J.P., Fidalgo, L.E., López-Beceiro, A. & Soler, F., 2007. Acetylcholinesterase activity in seabirds affected by the Prestige oil spill on the Galician coast (NW Spain). Science of the total environment, 372(2), pp.532-538.

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).

Heavy metal and arsenic content in seabirds affected by the Prestige oil spill on the Galician coast (NW Spain)

Pérez-López, M., Cid, F., Oropesa, A.L., Fidalgo, L.E., Beceiro, A.L. & Soler, F., 2006. Heavy metal and arsenic content in seabirds affected by the Prestige oil spill on the Galician coast (NW Spain). Science of the total environment, 359(1), pp.209-220.

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.

Population modelling of European shags (Phalacrocorax aristotelis) at their southern limit: conservation implications

Velando, A. and Freire, J., 2002. Population modelling of European shags (Phalacrocorax aristotelis) at their southern limit: conservation implications. Biological Conservation, 107(1), pp.59-69.


The European shag (Phalacrocorax aristotelis) population at Cíes Islands (the most important breeding area in its southern limit) increased rapidly from 1986 to 1992, and afterwards the population suffered a slight decline. This study analyzed population data obtained from ringing recoveries and reproductive monitoring between 1993 and 1997. The reproductive success was highly variable and associated with adverse weather events. Adult survival rate was very low compared with other colonies, probably due to high accidental capture in gill-nets. In recent years, the fishing effort with gill-nets increased in the study area. Sensitivity analysis of parameters showed that the population is more affected by changes in adult survival than in reproductive success. When dynamic simulations were run with an increase in shag mortality of 5% above the present level, population extinction occurred in all simulations. In contrast, when a reduction of mortality of 5% was introduced in the simulations, the population increased in all cases. The main lines of action to study and protect this population should be: (1) ringing schemes to obtain better estimates of survival variability; (2) studies on the interaction of feeding areas and fishing vessels; (3) regulations on gill-netting; and (4) the incorporation of population models as an adaptive management tool to synthesize assessment work and management scenarios.