Larus michahellis

Effects of testosterone implants on pair behaviour during incubation in the Yellow‐legged Gull Larus cachinnans

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Alonso‐Alvarez, C., 2001. Effects of testosterone implants on pair behaviour during incubation in the Yellow‐legged Gull Larus cachinnans. Journal of Avian Biology, 32(4), pp.326-332.

The Yellow-legged Gull Larus cachinnans is monogamous with bi-parental incubation. In this study, the effects of high levels of plasma testosterone in male Yellow-legged Gulls during the incubation period were analysed. Free-living male gulls were implanted with testosterone (T-males), and their sexual behaviour within the pair was observed and compared with that of control pairs. Egg temperatures, length of incubation and hatching success were also analysed. T-males and their mates displayed more sexual behaviour than the controls. T-males engaged in mounting behaviour with their mates, whereas control males did not. Proportionally less time was spent incubating (in relation to time present in the colony) by T-males than control males. However, the mates of T-males did not spend more time incubating than control females to compensate for male neglect, although they did spend more time on the territory. Egg temperature in T-male nests was significantly lower than in control nests, but no significant difference in the length of incubation or hatching success between the two groups was found. In birds, the effects of high testosterone levels on male behaviour during incubation have only been analysed in a polyandrous species whose females usually do not contribute to incubation. The present results thus suggest that those males of a monogamous species with biparental incubation that sustain high testosterone levels after laying, thus reducing their contributions to incubation, will be confronted with a lack of compensation from their mates during incubation. Finally, this lack of female compensation seems to be mediated by behavioural interactions with the male rather than by her absence
from the colony.

Female control in yellow-legged gulls: trading paternity assurance for food

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Velando, A., 2004. Female control in yellow-legged gulls: trading paternity assurance for food. Animal Behaviour, 67(5), pp.899-907.

Females in many socially monogamous birds copulate hundreds of times more than necessary for fertilization, although little is known about the benefits of this excess. Females may not directly benefit from high copulation rates, but instead may exploit male interest in copulating to obtain benefits. In species with courtship feeding, females may trade copulations for food (immediate benefits hypothesis). I tested this hypothesis by analysing female behaviour during courtship in yellow-legged gulls, Larus cachinnans. Female gulls to some extent controlled sperm transfer, because they moved during copulation bouts, and this behaviour influenced the number of cloacal contacts per mounting that the male achieved. Female control was related to previous feeding by the male, and hence the male courtship feeding rate correlated with the cloacal contact rate. Males that give more food probably enhance their chances of fathering offspring. By analysing within-individual female behaviour, I also found that the number of cloacal contacts was higher when the male fed the female than when he did not, which indicates that female gulls followed a decision rule to resist copulation when food is not given. Overall, these results support the hypothesis that female gulls manipulate their mates to obtain food.

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

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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

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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

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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

Distribution and partitioning of organic pollutants and effects in coastal birds

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Vicente de Bobes, J., 2014. Distribution and partitioning of organic pollutants and effects in coastal birds. Tesis Universitat Politècnica de Catalunya. Departament d’Enginyeria Hidràulica, Marítima i Ambiental. B 13734-2014

Les zones costaneres són unes àrees molt sensibles a la contaminació degut a la interacció entre els processos marins i antropogènics. Els emissaris submarins, les desembocadures dels rius, les activitats portuàries, l’abocament de residus, l’aqüicultura, etc. Són algunes de les activitats que poden produir la contaminació de les zones costaneres. Entre d’altres tipus de contaminants, es troben els contaminants orgànics persistents (COPs), aquells compostos orgànics que, en diferent grau, presenten resistència a la fotòlisis, la degradació química i la biològica. Degut a les seves característiques fisico-químiques, els COPs estan distribuïts per tot el món, podent trobar-se fins i tot en zones prístines molt allunyades de la seva font d’emissió original. Aquests contaminants tendeixen a bioacumular-se al llarg de les cadenes tròfiques, de manera que els grans depredadors són més sensibles a aquesta contaminació. Les aus marines estan molt exposades als contaminants orgànics degut als seus hàbits alimentaris i a la seva esperança de vida relativament llarga. En aquesta tesi s’ha estudiat l’acumulació de vàries famílies de contaminants orgànics en dues espècies de gavina de la Península Ibèrica, el gavià argentat (Larus michahellis) i la gavina corsa (L. audouinii). El gavià argentat és una gavina de grans dimensions molt comuna a la Península Ibèrica. És una espècie omnívora i oportunista. S’alimenta tant de recursos marins, com terrestres, com depredant sobre altres aus i també freqüenta abocadors i descarts pesquers. La gavina corsa és una gavina de dimensions mitjanes, endèmica de la regió mediterrània. Fa uns anys estava en situació de risc però el fort creixement poblacional de les últimes dècades l’ha deixat fora de perill sent considerada actualment a nivell internacional com a “quasi amenaçada”. És una espècie piscívora però cada vegada explota més descarts pesquers. En el primer estudi s’analitzen 6 famílies de contaminants orgànics inclosos o sota consideració pel Conveni d’Estocolm (els PCDD/Fs, PBDEs, PCBs, OCs, PFASs i SCCPs) en els ous de les dues espècies de gavina de les respectives colònies del Parc Natural del Delta de l’Ebre. A partir d’aquí els següents treballs es basen en l’estudi de la família dels PFASs en sang i ous d’ambdues espècies i pertanyents a diferents colònies de la Península Ibèrica (Delta de l’Ebre, Illes Medes, Illes Columbretes, Illa de Sa Dragonera, Illa Grosa, Illes Chafarinas, Illes Atlàntiques de Galicia i Ilhas Berlengas), totes en zones d’alt interès ecològic i sota alguna protecció ambiental (parcs naturals, nacionals, reserves marines, reserva de la biosfera, etc.). A partir dels nivells de PFASs trobats en les diferents matrius (primers ous de la posta, clara i rovell d’ou dels 3 ous de la posta i sang d’exemplars adults) s’estudia l’efecte d’aquests contaminants a nivell físic (paràmetres biomètrics de l’ou, gruix de la closca i índex de dessecació) i hormonal (via l’anàlisi de les hormones esteroidees 17β-estadiol i testosterona). S’estudia també l’acumulació d’aquests contaminants a partir de la dieta (analitzant el seu propi aliment i a partir de l’estudi dels isòtops estables de carboni i nitrogen (δ13C i δ15N), indicadors del règim alimentari) i es fa una estima de la depuració dels PFASs en sang i de la seva transferència de femelles a ous. Els resultats indiquen que els contaminants orgànics són presents en les poblacions de gavià argentat i gavina corsa de la Península Ibèrica, sent els OCs i els PCBs les famílies de compostos amb concentracions més elevades. Entre els PFASs, el compost majoritari és el PFOS. La transferència de contaminants orgànics de mares a cries queda demostrada amb els nivells trobats en els ous d’ambdues espècies. De l’anàlisi de PFASs en sang de mascles i femelles de les dues espècies de gavina s’observa que les femelles descarreguen part dels compostos acumulats als ous presentant així nivells en sang inferior que els mascles. No es troba cap relació entre els nivells de PFASs i els paràmetres biomètrics, com tampoc amb els nivells d’esteroides. Tanmateix, l’estudi de les hormones permet comparar els nivells en ambdues espècies amb altres estudis i discutir la influència de la dieta. L’anàlisi de PFASs en clara i rovell d’ou per separat dels 3 ous de les postes de gavina corsa demostren que aquests compostos tenen més afinitat pels lípids del rovell ja que no es detecten en les clares. La concentració decreixent de PFOS al llarg de la seqüència de posta demostra que les femelles descarreguen la majoria de contaminant en el primer ou però que existeix una bona correlació dels nivells de PFOS entre els 3 ous d’un mateix niu. L’augment de les concentracions d’alguns PFASs en el 3r ou i les diferències en els valors de δ13C entre el 1r-3r i 2n-3r ou s’atribueixen a l’anomenat “efecte mare” (possible ús de reserves endògenes per a la formació de l’últim ou enlloc de l’energia aportada per la dieta prèvia a la posta). Aquesta tesi permet augmentar el coneixement sobre l’acumulació de COPs en el gavià argentat i la gavina corsa de la Península Ibèrica, avaluar les diferències entre ambdues espècies i associar-ho a la seva biologia, determinar la distribució geogràfica de COPs utilitzant els ous com a bioindicador de contaminació ambiental i estudiar els processos d’acumulació i transferència de PFASs.

Dioxins and dl-PCBs in gull eggs from Spanish Natural Parks (2010–2013)

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Morales, L., Martrat, M.G.R., Parera, J., Bertolero, A., Ábalos, M., Santos, F.J., Lacorte, S. & Abad, E., 2016. Dioxins and dl-PCBs in gull eggs from Spanish Natural Parks (2010–2013). Science of the Total Environment, 550, pp.114-122.

The aim of this study was to evaluate the presence and distribution of polychlorinated dibenzo-p-dioxins, dibenzofurans (PCDD/Fs) and biphenyls (PCBs), concretely those so-called as dioxin-like PCBs, in yellow-legged gull eggs (Larus michahellis) collected from five Natural Parks (some of them National Parks) in Spain during the period 2010–2013. PCDD/Fs and dl-PCBs were detected in all the samples. Due to the proximity to important urban and industrial areas higher concentrations were determined in colonies located in the Northern Mediterranean coast than those found in the Southern Mediterranean or Atlantic colonies where a softer anthropogenic impact occurs. Mean ∑ PCDD/F concentrations ranged from 49 to 223 pg/g lipid weight (lw) and ∑ dl-PCB concentrations varied from 146 to 911 ng/g lw. In the Natural Park of the Ebro Delta (Northern Mediterranean coast) two gull species share habitat: yellow-legged and Audouin gull (Larus audouinii). Eggs from both species were collected and PCDD/F and dl-PCB levels compared. The species that feeds exclusively on pelagic fish (L. audouinii) had significantly higher PCDD/F and dl-PCB levels than the scavenger L. michahellis, pointing out the diet-dependent differences in the accumulation of persistent organic pollutants between similar cohabitant breeding species. Finally, mean TEQ values were in general below those considered as critical for toxicological effects in birds.

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

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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

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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.

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

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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.