Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks

Eggs of vertebrates contain steroid hormones of maternal origin that may influence offspring performance. Recently, it has been shown that glucocorticoids, which are the main hormones mediating the stress response in vertebrates, are transmitted from the mother to the egg in birds. In addition, mothers with experimentally elevated corticosterone levels lay eggs with larger concentrations of the hormone, which produce slow growing offspring with high activity of the hypothalamo-adrenal axis under acute stress. However, the effects and function of transfer of maternal corticosterone to the eggs are largely unknown. In the present study, we injected corticosterone in freshly laid eggs of yellow-legged gulls (Larus michahellis), thus increasing the concentration of the hormone within its natural range of variation, and analyzed the effect of manipulation on behavioral, morphological, and immune traits of the offspring in the wild. Eggs injected with corticosterone had similar hatching success to controls, but hatched later. Mass loss during incubation was greater for corticosterone-treated eggs, except for the last laid ones. Corticosterone injection reduced rate and loudness of late embryonic vocalizations and the intensity of chick begging display. Tonic immobility response, reflecting innate fearfulness, was unaffected by hormone treatment. Elevated egg corticosterone concentrations depressed T-cell-mediated immunity but had no detectable effects on humoral immune response to a novel antigen, viability at day 10, or growth. Present results suggest that egg corticosterone can affect the behavior and immunity of offspring in birds and disclose a mechanism mediating early maternal effects whereby stress experienced by females may negatively translate to offspring phenotypic quality.     

Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks

Maternal effects mediated by egg quality are important sources of offspring phenotypic variation and can influence the course of evolutionary processes. Mothers allocate to the eggs diverse antioxidants that protect the embryo from oxidative stress. In the yellow-legged gull (Larus michahellis), yolk antioxidant capacity varied markedly among clutches and declined considerably with egg laying date. Analysis of bioptic yolk samples from clutches that were subsequently partially cross-fostered revealed a positive effect of yolk antioxidant capacity on embryonic development and chick growth, but not on immunity and begging behaviour, while controlling for parentage and common environment effects. Chick plasma antioxidant capacity varied according to rearing environment, after statistically partitioning out maternal influences mediated by egg quality. Thus, the results of this study indicate that egg antioxidants are important mediators of maternal effects also in wild bird populations, especially during the critical early post-hatching phase.     

Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow-legged gull (Larus michahellis) chicks in relation to sex and laying order

Egg quality may mediate maternal allocation strategies according to progeny sex. In vertebrates, carotenoids have important physiological roles during embryonic and post-natal life, but the consequences of variation in yolk carotenoids for offspring phenotype in oviparous species are largely unknown. In yellow-legged gulls, yolk carotenoids did not vary with embryo sex in combination with egg laying date, order and mass. Yolk lutein supplementation enhanced the growth of sons from first eggs but depressed that of sons from last eggs, enhanced survival of daughters late in the season, and promoted immunity of male chicks and chicks from small eggs. Lack of variation in egg carotenoids in relation to sex and egg features, and the contrasting effects of lutein on sons and daughters, do not support the hypothesis of optimal sex-related egg carotenoid allocation. Carotenoids transferred to the eggs may rather result from a trade-off between opposing effects on sons or daughters.     

Influence of host age and sex on the helminth fauna of the yellow-legged gull (Larus michahellis) in Galicia (northwestern Spain)

We studied the influence of host age and sex on the helminth fauna of 324 Larus michahellis captured in different locations in the region of Galicia (northwestern Spain). Gulls were grouped into prefledglings, first-year immature birds, second- and third-year immature birds, and adults. Second-year, third-year, and adult birds were grouped by sex. Thirty-six helminth species were recorded. Total species richness and mean infracommunity species richness were both significantly lower for pre-fledglings than for the other age groups. Prevalence increased significantly with age for Brachylecithum microtesticulatum, probably reflecting changing feeding habits. Likewise, 8 species (Cardiocephaloides longicollis, Microphallus similis, Maritrema gratiosum, Gynaecotyla longiintestinata, Brachylecithum microtesticulatum, Himasthla elongata, Parorchis acanthus, and Renicola sp.) were absent or had very low prevalence in prefledglings. At least 5 of these 8 species are transmitted to gulls through ingestion of molluscs or crustaceans, which suggests that these types of prey are seldom fed to prefledglings. In Gymnophallus deliciosus, G. longiintestinata, and Cosmocephalus obvelatus, mean intensity, and in the latter case prevalence, declined with age, suggesting that protective immunity against these species increase with age. Only G. deliciosus, Microphallus similis, and G. longiintestinata presented significant differences between the sexes.     

Phenotypic correlates of yolk and plasma carotenoid concentration in yellow-legged gull chicks

Abstract Carotenoids perform important biological actions in animal tissues, including contributing antioxidant protection. However, the function of transmission of maternal carotenoids to bird eggs is still largely unknown. We made a yolk biopsy of yellow-legged gull (Larus michahellis) eggs and found that the concentration of lutein declined with laying date and across the laying order and increased with egg mass. The concentration of all the main carotenoids (lutein, zeaxanthin, and dehydrolutein) pooled also declined with date and increased with egg mass. We also performed a partial reciprocal cross-fostering of eggs between clutches and investigated the covariation between morphology, T cell-mediated immunity, and plasma carotenoid concentrations of the chicks and carotenoid concentrations in their original eggs. Absolute plasma carotenoid concentrations did not covary with those in the yolk, whereas a positive covariation was found for relative concentrations. Yolk and absolute plasma carotenoid concentrations positively predicted chick body mass and size but not the intensity of the cell-mediated immune response. Thus, yolk carotenoid concentrations may affect chick carotenoid profile and growth, possibly mediating early maternal effects. However, rearing conditions also contributed to determining relative concentrations of circulating carotenoids. Since yolk or plasma antioxidant capacity did not correlate with carotenoid concentrations, future studies of maternal effects mediated by antioxidants should integrate information on carotenoids with information on other components of the antioxidant systems.     

Hepatotoxic effect of metallic pollutants on enzyme histochemical activities of yellow-legged gull Larus cachinnans michahellis liver.

We studied the hepatotoxic effect of heavy metals (cadmium, mercury, copper) on Mg2+ -ATPase, NADH diaphorase, succinic dehydrogenase and acid phosphatase of yellow-legged gull liver, using enzyme histochemical methods. The lysosomal enzyme activity of acid phosphatase was increased in all cases. However, the other enzyme activities appeared to be insensitive to the different metallic pollutants and to their respective levels, in contrast with literature experimental data showing plasma membrane and mitochondrial alterations. This controversy could be explained by the differences in dietary conditions and metal overloads. The molecular basis of the toxicities of metallic pollutants is discussed.     

Maternal yolk androgens stimulate territorial behaviour in black-headed gull chicks

Avian eggs contain substantial amounts of maternal androgens. The concentrations of these yolk androgens are affected by the maternal environment, such as the level of social competition, parasite exposure or food conditions. Since yolk androgens have been shown to affect a wide array of offspring traits, they may adjust the chicks to the expected post-hatching environment, but experimental evidence is still scarce. We investigate in colonial breeding black-headed gulls whether high concentrations of yolk androgens, such as those found in environments with high numbers of social interactions, facilitate aggressiveness and territorial behaviour of the chicks. Black-headed gulls are highly suitable for this, as the semi-precocial chicks defend the natal territory and food against intruders. We manipulated yolk androgen concentrations and investigated their role in both within-nest and between-nest aggression. We found that chicks hatching from androgen-treated eggs defended the natal territory more often than their nest mates from control eggs, without increasing sibling aggression. This suggests that variation in yolk androgen concentrations in relation to the social environment of the mother may indeed allow adjustment of the offspring''s behaviour to the expected frequency of territorial interactions with conspecifics post-hatching.     

Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study

Black-headed gulls, Larus ridibundus, produce clutches of three eggs, which contain high levels of maternal androgens in the yolk. These levels increase with laying order and the eggs hatch asynchronously. Experiments have supported the hypothesis that this within-clutch variation in maternal androgens mitigates the disadvantage of last-hatched chicks in sibling competition, by enhancing embryonic development and early posthatching growth. We hypothesized that these effects come about by the stimulating effects of maternal androgens on begging behaviour and competitive ability. In the field, we injected first-laid eggs of a clutch (which have a low androgen level) with either an androgen solution (T eggs) or vehicle (Oil eggs). We then created pairs of chicks hatched from Oil and T eggs, matched for egg mass and hatching date. Parent-chick interactions were recorded from observation hides. Chicks from T eggs hatched almost half a day sooner than those from Oil eggs. Furthermore, chicks from T eggs were more active during the first week after hatching, were more often the first to react to the approaching parent, begged more frequently, and obtained the larger share of food. We conclude that the enhancing effect of yolk androgens on growth in this species arises at least partly through androgen-mediated effects on the chicks' behaviour. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: the yellow-legged gull Larus michahellis

Female birds transfer antibodies to their offspring via the egg yolk, thus possibly providing passive immunity against infectious diseases to which hatchlings may be exposed, thereby affecting their fitness. It is nonetheless unclear whether the amount of maternal antibodies transmitted into egg yolks varies with female quality and egg laying order. In this paper, we investigated the transfer of maternal antibodies against type A influenza viruses (anti-AIV antibodies) by a long-lived colonial seabird, the yellow-legged gull (Larus michahellis), in relation to fluctuating asymmetry in females, i.e. the random deviation from perfect symmetry in bilaterally symmetric morphological and anatomical traits. In particular, we tested whether females with greater asymmetry transmitted fewer antibodies to their eggs, and whether within-clutch variation in yolk antibodies varied according to the maternal level of fluctuating asymmetry. We found that asymmetric females were in worse physical condition, produced fewer antibodies, and transmitted lower amounts of antibodies to their eggs. We also found that, within a given clutch, yolk antibody level decreased with egg laying order, but this laying order effect was more pronounced in clutches laid by the more asymmetric females. Overall, our results support the hypothesis that maternal quality interacts with egg laying order in determining the amount of maternal antibodies transmitted to the yolks. They also highlight the usefulness of fluctuating asymmetry as a sensitive indicator of female quality and immunocompetence in birds.     

Sex differences in growth rates of Yellow-legged Gull Larus michahellis chicks

Capsule: Chick growth rates was sex-dependent in an Atlantic Yellow-legged Gull Larus michahellis population.

Aims: To describe the growth rate of Yellow-legged Gull chicks and sex-associated variations, and obtain a discriminant function to sex them using morphological data.

Methods: Fifty-two Yellow-legged Gull chicks from a colony in northern Iberia were measured for body mass, head and bill length, tarsus length and three other bill-length associated variables, from the hatching date up to the age of 36 days. Birds were sexed using DNA analysis.

Results: Using logistic models, chick growth rates was observed to be similar between the sexes, while the asymptote was higher among males for the majority of the variables. Discriminant analyses showed that the variable head+bill was very reliable to predict the sex of >80% of chicks at an early developmental stage, and 100% of chicks if combined with tarsus length and two more bill-length associated variables at the age of 35 days.

Conclusions: This is the first study using a discriminant analysis to sex Yellow-legged Gull chicks, and also the first to describe the growth function for the species. The growth rate varied between sexes because males showed higher asymptote values within the growth function.     

Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus)

It has been proposed that the maternal androgens in avian egg yolk enhance offspring fitness by accelerating growth and improving competitive ability. Because egg quality is strongly influenced by maternal condition, we predicted that females in good condition would produce high-quality eggs with relatively high androgen content. We experimentally enhanced maternal condition by supplementary feeding lesser black-backed gulls (Larus fuscus) during egg formation and compared the concentrations of androstenedione (A4), 5alpha-dihydrotestosterone (DHT) and testosterone (T) in their eggs with those in eggs laid by control females. We also measured circulating levels of T in females immediately after laying. Egg androgens could affect offspring performance directly through chick development and/or indirectly through changes in the competitive ability of a chick relative to its siblings. To avoid confounding these two routes, and to separate effects operating through the egg itself with those operating through experimental changes in parental chick rearing capacity, we fostered eggs from both maternal treatment groups singly into the nests of unmanipulated parents. Contrary to expectation, mothers with experimentally enhanced body condition laid eggs with lower levels of androgens, while exhibiting higher circulating T concentrations post-laying. Despite these lower levels of egg androgen, offspring hatched from eggs laid by mothers in good condition did not show reduced growth or survival when reared in the absence of sibling competition. Our results demonstrate that yolk androgen concentrations vary with the body condition of the female at the time of egg formation and that females in good condition reduced the yolk androgen content of their eggs without altering offspring performance.     

The hormonal control of begging and early aggressive behavior: experiments in black-headed gull chicks

The hormonal control of begging and sibling competition is largely unknown, but recent evidence suggests a role for steroid hormones. We tested the influence of the aromatizable androgen testosterone (T), the non-aromatizable androgen 5alpha-dihydrotestosterone (DHT), and 17beta-estradiol (E) on both begging behavior and aggressive behavior in black-headed gull chicks (Larus ridibundus). Chicks of this species have a conspicuous begging display, while their frequently performed early aggressive behavior is facilitated by testosterone and important for territorial defense. Hormone treatment was applied by implants between days 6 and 16 after hatching. Behavior was tested by means of standard stimulus tests. The results were validated in a second experiment under semi-natural conditions. Begging was suppressed by T and DHT and not affected by E. Aggressive Pecking was strongly facilitated by T. The erect threat posture, characteristic for older chicks, was facilitated by T, DHT, and E and the nest-oriented threat display, typical for young chicks, only by T and DHT. Growth was suppressed in the T group. The results indicate that androgen production, needed for territorial defense, has costs in terms of a suppression of begging and growth. It is discussed to what extent older chicks may avoid these costs by converting testosterone to estrogen and why pre-natal and post-natal exposure to androgens differ in their effect on begging behavior.     

Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development

We tested the hypothesis that mother birds counterbalance the negative effects of hatching asynchrony for later-hatched chicks by increasing the yolk androgen concentrations in consecutive eggs of their clutch. In doing so, they may adaptively tune each offspring's competitive ability and, thus, growth and survival. However, evidence in support of this hypothesis is contradictory. The yolk concentrations of maternal androgens in the eggs of black-headed gulls increase significantly with the laying order of the eggs in a clutch. We experimentally tested the functional consequences of this increase on chick development under natural conditions by injecting eggs with either an oil or androgen solution. We created experimental clutches in which androgen levels either stayed constant or increased with laying order while controlling for differences in egg quality by using only first-laid eggs. We then compared development, growth and survival between these broods. Androgen treatment enhanced embryonic development because androgen-treated eggs hatched half a day earlier than controls, while their size at hatching was similar to oil-treated controls. Androgen treatment did not increase chick survival, but it enhanced growth. Androgen-treated, third-hatched chicks had a higher body mass and longer legs than third-hatched chicks that hatched from oil-treated eggs. At the same time, growth of first chicks (which were all oil treated) was reduced by the presence of two androgen-treated siblings, suggesting that yolk androgens enhance the competitive ability of later-hatched chicks. Our results support the hypothesis that transfer of different amounts of androgens to the eggs of a clutch is a mechanism by which mothers maximize their reproductive output.     

Helminth fauna of the yellow-legged gull Larus cachinnans in Galicia, north-west Spain

Thirty-six helminth species were found in 324 gulls examined during June 1994 to February 1996 from different localities of Galicia: 25 trematodes (Brachylaima sp., Brachylecithum microtesticulatum, Cardiocephaloides longicollis, Cryptocotyle lingua, Cryptocotyle concavum, Diplostomum spathaceum, Echinostephilla virgula, Galactosomum phalacrocoracis, Gigantobilharzia acotylea, Gymnophallus deliciosus, Gynaecotyla longiintestinata, Himasthla elongata, Himasthla quissetensis, Knipowitschiatrema nicolai, Levinseniella (Levinseniella) propinqua, Maritrema gratiosum, Maritrema linguilla, Microphallus primas, Microphallus similis, Ornithobilharzia canaliculata, Parorchis acanthus, Phagicola minuta, Psilostomum brevicolle, Renicola sp. and Stephanoprora denticulata), four cestodes (Alcataenia micracantha, Microsomacanthus ductilis, Tetrabothrius (Oriana) erostris and Wardium cirrosa), six nematodes (Anisakis simplex, Contracaecum rudolphii, Cosmocephalus obvelatus), Eucoleus contortus, Paracuaria adunca and Tetrameres (Tetrameres) skrjabini) and one acanthocephalan (Arhythmorhynchus longicollis). Tetrabothrius erostris was the most prevalent species (79.6%), followed by C. obvelatus (47.8%), C. lingua (37.4%), G deliciosus (30.9%), G. longiintestinata (22.8%), P. adunca (21.9%), B. microtesticulatum (17.6%), E. contortus (14.5%) and M. similis (9.3%). Microphallus similis was the dominant species, with a Berger-Parker index (BP) of 0.32, followed by T. erostris (BP=0.10). All species presented an aggregated dispersion except G. acotylea and G. phalacrocoracis, which showed a random dispersion. Species that seem to have the greatest predilection for specific sites along the intestine are: C. longicollis and A. micracantha (first third), Brachylaima sp., M. similis and G. longiintestinata (last third) and A. longicollis (second half). Eight species are known to be pathogenic to commercially important fish or molluscan species and several are pathogenic to humans.     

Sex‐specific effects of yolk androgens on begging behavior and digestion in pied flycatchers

The hormonal environment during early development, such as maternally derived androgens in bird eggs, has been shown to shape offspring in ways that may have important short‐ and long‐term consequences for phenotype and behavior. However, studies on the effects of androgens on begging behavior and growth in birds have provided variable results and sex‐specific effects are not well understood. We experimentally elevated yolk androgen levels in whole clutches in a passerine bird, the pied flycatcher Ficedula hypoleuca and studied effects on male and female begging behavior, ingestion and digestion. Yolk androgen elevation led to shorter latencies to beg in both male and female nestlings but to greater begging rates only in males. Both responses could be used as cues to solicit more food from parents. Yolk androgens had no effect on food intake, fecal wet mass or fecal water content. However, the proportion of organic matter in feces was lower in androgen‐treated than control males, potentially suggesting that the androgen‐treated individuals had more efficient digestion. We discuss the alternative pathways of effects of yolk androgens on begging, growth and digestion. If the effects of yolk androgens on phenotype and behavior are causally linked, there is less scope for the mother to adjust specific offspring traits independently from other traits. The sex‐specific effects of yolk androgens should be studied more, also in within‐clutch context, as the costs and benefits for each sex may further differ in relation to hatching order.     

Hybridization of glaucous gull (Larus hyperboreus) and herring gull (Larus argentatus) in Iceland: mitochondrial and microsatellite data

Large white-headed gulls provide an interesting group of birds for studies of hybridization. The group is composed of 20 species of recent origin, often with weak reproductive barriers. Here we report the results from a study on the glaucous gull Larus hyperboreus, an Arctic species which has been breeding in Iceland for centuries, and the herring gull Larus argentatus which has a wide distribution in Europe but colonized Iceland in 1920s. Previous studies, based on morphological variation indicated hybridization between the two species in Iceland, have been questioned as it may just reflect variation within the species. Here we evaluate whether hybridization has occurred between the two species in Iceland by studying variation in microsatellites and mtDNA. The analysis is based on feathers taken from wings sampled in Iceland over a period of 40 years. The results are compared with samples obtained from East Greenland and published sequences of samples obtained throughout Europe. The genetic analysis reveals a distinctive grouping of the two species, although they present a shallow genealogy and an extensive sharing of the genetic variants between the two species. Several individuals show admixture for molecular markers, which may result from an incomplete lineage sorting although geographical patterns of both mtDNA haplotypes and microsatellites strongly indicate a recent hybridization in Iceland.