Family-transmitted stress in a wild bird

Noguera, J.C., Kim, S.Y. & Velando, A., 2017. Family-transmitted stress in a wild bird. Proceedings of the National Academy of Sciences, p.201706164. Proceedings of the National Academy of Sciences (PNAS): 201706164.


Recent data suggest that, in animals living in social groups, stress-induced changes in behavior have the potential to act as a source of information, so that stressed individuals could themselves act as stressful stimuli for other individuals with whom they interact repeatedly. Such form of cross-over of stress may be beneficial if it enhances adaptive responses to ecological stressors in the shared environment. However, whether stress can be transferred among individuals during early life in natural populations remains unknown. Here we tested the effect of living with stressed siblings in a gull species where, as in many vertebrates, family represents the basic social unit during development. By experimentally modifying the level of stress hormones (corticosterone) in brood mates, we demonstrate that the social transfer of stress level triggers similar stress responses (corticosterone secretion) in brood bystanders. Corticosterone-implanted chicks and their siblings were faster in responding to a potential predator attack than control chicks. In gulls, fast and coordinated reactions to predators may increase the chances of survival of the whole brood, suggesting a beneficial fitness value of cross-over of stress. However, our data also indicate that living with stressed brood mates early in life entails some long-term costs. Near independence, fledglings that grew up with stressed siblings showed reduced body size, high levels of oxidative damage in lipids and proteins, and a fragile juvenile plumage. Overall, our results indicate that stress cross-over occurs in animal populations and may have important fitness consequences.

Plumage colour and the expression of stress-related genes in gull chicks

Diaz-Real, J., Kim, S.Y. & Velando, A., 2017. Plumage colour and the expression of stress‐related genes in gull chicks. Journal of Avian Biology. DOI: 10.1111/jav.01460


In many bird populations, individuals show remarkable differences in feather colouration, which are often linked to individual differences in physiological traits, but the mechanisms maintaining this covariation are still unclear. Here, we investigate the variability of the melanic colouration in yellow-legged gull (Larus michahellis) chicks. In this species, hatchlings show high variability in the number and colour intensity of black spots in their plumage. In gulls, last-laid eggs receive less antioxidants but higher levels of androgens than first eggs. We first explored whether these remarkable differences within the clutch affect the feather melanisation during embryo development. Melanic colouration was not related to laying order, but nestling males were darker and had a larger spotted area than nestling females. In chicks hatching from first-laid eggs, the spot size and spot lightness were negatively correlated. We also explored the effect of the developmental environment, through a cross-fostering experiment, on the expression of five stress-related genes (SOD2, ALKBH3, HSPA8, NLRC5 and TRIAP1) and their link with melanic colouration. Post-hatching hierarchy did not affect the expression of any of the tested genes, but paler chicks showed reduced expression in some studied genes (SOD2, ALKBH3 and HSPA8) in comparison to darker chicks. Our results suggest that melanic chicks suffer less stress during development.

On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks

Noguera, J.C., Morales, J., Pérez, C. & Velando, A., 2010. On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks. Behavioral Ecology, 21(3), pp.479-484.


Offspring solicit food to their parents by begging displays, which are important in the parent–offspring communication. Most theoretical approximations on this behavior have centered on the view of begging as an honest signal of need or as a form of scramble competition for resources. In both signaling models, costly begging is necessary to stabilize the begging strategy at equilibrium. Nevertheless, evidence supporting begging as costly behavior remains scarce. We investigated whether oxidative stress may represent a general form of proximate cost of begging and also whether begging is related to offspring nutritional condition. To test this, we experimentally modified the chicks’ nutritional condition and vitamin E availability and measured the effects on different begging components. The intensity of all begging components increased in chicks that were intake restricted, whereas vitamin E specifically enhance the total number of chatter calls given by chicks, mainly in those with a lower body size. Our results suggest that begging behavior is an antioxidant demanding activity and support the idea that oxidative stress may be a cost of begging. Our findings also suggest that begging behavior may be an honest signal of the nutritional and oxidative status of the chicks.

The evolution of multicomponent begging display in gull chicks: sibling competition and genetic variability

Kim, S.Y., Noguera, J.C., Morales, J. & Velando, A., 2011. The evolution of multicomponent begging display in gull chicks: sibling competition and genetic variability. Animal Behaviour, 82(1), pp.113-118.

The evolution of begging display may be influenced by gene–environment interaction, through the mechanisms that adjust begging behaviour to environmental conditions of offspring, including intensity of sibling competition within broods. We decomposed the complex begging display of yellow-legged gull, Larus michahellis, chicks into two different functional components: begging for food (pecks) and drawing the attention of parents (chatter calls). We examined these begging components in 2-day-old chicks that hatched and grew up in foster nests, by performing a begging test for each chick alone without the hindrance of its foster siblings. Male chicks and those with poorer body condition begged for food at higher rates than females and those with better body condition, respectively. Chicks from larger broods begged for food more frequently, but chicks from male-biased broods begged less frequently. If begging is costly, chicks may adjust their begging efforts to the intensity of sibling competition. Frequency of chatter calls varied with sex, chick order within broods and body condition: females, the third chicks and those with poorer condition produced chatter calls more frequently. Genetic origin had a significant effect on frequency of chatter calls but not on begging for food, while foster nest effect was null in both traits. Therefore, chatter calls (but not pecks) can be subject to evolution under directional selection. Different begging components may have evolved through different evolutionary pathways.

Yolk testosterone reduces oxidative damages during postnatal development

Noguera, J.C., Alonso-Alvarez, C., Kim, S.Y., Morales, J. & Velando, A., 2011. Yolk testosterone reduces oxidative damages during postnatal development. Biology letters, 7(1), pp.93-95.


Conditions experienced during early life can influence the development of an organism and several physiological traits, even in adulthood. An important factor is the level of oxidative stress experienced during early life. In birds, extra-genomic egg substances, such as the testosterone hormone, may exert a widespread influence over the offspring phenotype. Interestingly, testosterone can also upregulate the bioavailability of certain antioxidants but simultaneously increases the susceptibility to oxidative stress in adulthood. However, little is known about the effects of maternally derived yolk testosterone on oxidative stress in developing birds. Here, we investigated the role of yolk testosterone on oxidative stress of yellow-legged gull chicks during their early development by experimentally increasing yolk testosterone levels. Levels of antioxidants, reactive oxygen species and lipid oxidative damage were determined in plasma during nestlings’ growth. Our results revealed that, contrary to control chicks, birds hatched from testosterone-treated eggs did not show an increase in the levels of oxidative damage during postnatal development. Moreover, the same birds showed a transient increase in plasma antioxidant levels. Our results suggest that yolk testosterone may shape the oxidative stress-resistance phenotype of the chicks during early development owing to an increase in antioxidant defences and repair processes.

Hatching hierarchy but not egg-related effects governs behavioral phenotypes in gull chicks

Diaz-Real, J., Kim, S.Y. & Velando, A., 2016. Hatching hierarchy but not egg-related effects governs behavioral phenotypes in gull chicks. Behavioral Ecology. doi: 10.1093/beheco/arw110


In many bird species that practice parental care, siblings often compete for resources and care provided by their parents, although their strategies differ according to hatching rank and condition. Differences in offspring strategies are generally attributed to hatching order and maternal effects, which are difficult to separate because these effects are often correlated. For example, third-hatched chicks of large gull species receive more egg testosterones and corticosterone, which influence early behavioral patterns. In this study, we carried out a cross-fostering experiment with first- and last-laid eggs of the yellow-legged gull (Larus michahellis) to test whether the within-brood variation in behavioral strategies for competing with siblings and coping with stress are due to maternal effects or to hatching order. Chicks hatched in the last position within the experimental brood emitted more chatter calls to attract parents’ attention, were less prone to respond to warning of danger, and had a lower breathing rate while restrained than first-hatched chicks. Egg laying order did not affect chick behaviors or breathing rate. Thus, we concluded that the different behavioral strategies of chicks were determined by their posthatching experience and not by the original egg position within the clutch. Last-laid eggs were smaller and chicks from those eggs grew slower than chicks from first-laid eggs. Independently of the original laying order, chicks that hatched first in the experimental brood grew faster than their siblings. Overall, our results indicate that behavioral strategies of chicks are plastic and influenced by their early social

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.