Effects of elevated yolk androgens on perinatal begging behavior in yellow-legged gull (Larus michahellis) chicks

Maternal hormones may represent an important pathway by which mothers can adaptively adjust offspring traits and performance to suit the prevailing environmental conditions. Earlier studies of birds have shown that egg androgens of maternal origin may enhance post-natal offspring 'begging' displays, functioning to solicit parental care. Here we investigate the effects of elevated egg androgen levels on the prenatal begging behavior of yellow-legged gull (Larus michahellis) chicks. At laying, we experimentally increased the concentration of yolk testosterone (T) within the natural range of variation, and, shortly before hatching, we compared the structural properties, rate, and loudness of vocalizations of embryos developing in T- and oil-injected (control) eggs. In addition, we compared the early post-hatch begging rate (measured as the pecking rate towards a dummy gull head) in chicks of the two experimental groups. We found that T embryos produced louder embryonic vocalizations than controls, whereas structural properties and the calling rate did not differ between T and control embryos. The post-hatch begging rate was unaffected by T treatment, but strongly decreased with increasing chick body mass, suggesting that intensity of the begging display was sensitive to chick state and may therefore reliably indicate the need of food in this species. Therefore, the results of this study show for the first time that prenatal T exposure modulates the quality of embryonic vocalizations, but are not in accordance with previous findings reporting increased post-hatching begging intensity following increased prenatal exposure to androgens.     

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.     

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.     

Maternal effects mediated by egg quality in the Yellow-legged Gull Larus michahellis in relation to laying order and embryo sex

Background

Maternal effects mediated by egg size and quality may profoundly affect offspring development and performance, and mothers may adjust egg traits according to environmental or social influences. In avian species, context-dependency of maternal effects may result in variation in egg composition, as well as in differential patterns of covariation among selected egg components, according to, for example, position in the laying sequence or offspring sex. We investigated variation in major classes of egg yolk components (carotenoids, vitamins and steroid hormones) in relation to egg size, position in the laying sequence and embryo sex in clutches of the Yellow-legged Gull (Larus michahellis). We also investigated their covariation, to highlight mutual adjustments, maternal constraints or trade-offs in egg allocation.

Results

Laying sequence-specific patterns of allocation emerged: concentration of carotenoids and vitamin E decreased, while concentrations of androgens increased. Vitamin A, estradiol and corticosterone did not show any change. There was no evidence of sex-specific allocation or covariation of yolk components. Concentrations of carotenoids and vitamins were positively correlated. Egg mass decreased along the laying sequence, and this decrease was negatively correlated with the mean concentrations of carotenoids in clutches, suggesting that nutritionally constrained females lay low quality clutches in terms of carotenoid content. Finally, clutches with smaller decline in antioxidants between first- and last-laid eggs had a larger increase in yolk corticosterone, suggesting that a smaller antioxidant depletion along the laying sequence may entail a cost for laying females in terms of increased stress levels.

Conclusions

Since some of the analyzed yolk components (e.g. testosterone and lutein) are known to exert sex-specific phenotypic effects on the progeny in this species, the lack of sex-specific egg allocation by mothers may either result from trade-offs between contrasting effects of different egg components on male and female offspring, or indicate that sex-specific traits are controlled primarily by mechanisms of sexual differentiation, including endogenous hormone production or metabolism of exogenous antioxidants, during embryonic development.     

Human fluctuating asymmetry in relation to health and quality: a meta-analysis

Developmental instability (DI) reflects the inability of a developing organism to buffer its development against random perturbations, due either to frequent, large perturbations or to a poor buffering system. The primary measure used to assess DI experienced by an individual organism is fluctuating asymmetry (FA), asymmetry of bilateral features that are, on average in a population, symmetrical. A large literature on FA in humans in relation to measures of health and quality (close to 100 studies and nearly 300 individual effect size estimates) has accumulated. This paper presents the first quantitative meta-analysis of this literature. The mean effect size (scaled as Pearson r) was about 0.2. Effect sizes covaried negatively with sample size, consistent with effects of publication bias, the tendency for significant effects to be published. Conservative correction for this bias reduced the mean effect to about 0.1. Associations with FA underestimate effects of underlying DI due to imprecise measurement of the latter. A model-based best estimate of the mean effect of DI on outcomes is about 0.3, a theoretically meaningful, relatively large effect, albeit of moderate absolute size. The data are consistent, however, with a range of true effect sizes between 0.08 and 0.67, partly due to large study effects. Study-specific effect sizes in DI ranged between −0.2 and 1.0. A humbling and perhaps sobering conclusion is that, in spite of a large body of literature involving nearly 50 000 participants, we can only confidently state that there is on average a robust positive average effect size. An accurate estimate of that effect size was not possible, and between-study variation remained largely unexplained. We detected no robust variation across six broad categories of outcomes (health and disease, fetal outcomes, psychological maladaptation, reproduction, attractiveness and hormonal effects), though examination of narrower domains reveal some corrected effects close to 0.2 and others near zero. The meta-analysis suggests fruitful directions for future research and theory.     

Egg production in a coastal seabird, the glaucous-winged gull (Larus glaucescens), declines during the last century

Seabirds integrate information about oceanic ecosystems across time and space, and are considered sensitive indicators of marine conditions. To assess whether hypothesized long-term foodweb changes such as forage fish declines may be reflected in a consumer's life history traits over time, I used meta-regression to evaluate multi-decadal changes in aspects of egg production in the glaucous-winged gull (Larus glaucescens), a common coastal bird. Study data were derived from literature searches of published papers and unpublished historical accounts, museum egg collections, and modern field studies, with inclusion criteria based on data quality and geographic area of the original study. Combined historical and modern data showed that gull egg size declined at an average of 0.04 cc y(-1) from 1902 (108 y), equivalent to a decline of 5% of mean egg volume, while clutch size decreased over 48 y from a mean of 2.82 eggs per clutch in 1962 to 2.25 in 2009. There was a negative relationship between lay date and mean clutch size in a given year, with smaller clutches occurring in years where egg laying commenced later. Lay date itself advanced over time, with commencement of laying presently (2008-2010) 7 d later than in previous studies (1959-1986). This study demonstrates that glaucous-winged gull investment in egg production has declined significantly over the past ～50-100 y, with such changes potentially contributing to recent population declines. Though gulls are generalist feeders that should readily be able to buffer themselves against food web changes, they are likely nutritionally constrained during the early breeding period, when egg production requirements are ideally met by consumption of high-quality prey such as forage fish. This study's results suggest a possible decline in the availability of such prey, and the incremental long-term impoverishment of a coastal marine ecosystem bordering one of North America's rapidly growing urban areas.     

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.     

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.     

High connectivity in a long-lived high-Arctic seabird,the ivory gull <Emphasis Type="Italic">Pagophila eburnea</Emphasis>

Species may cope with rapid habitat changes by distribution shifts or adaptation to new conditions. A common feature of these responses is that they depend on how the process of dispersal connects populations, both demographically and genetically. We analyzed the genetic structure of a near-threatened high-Arctic seabird, the ivory gull (Pagophila eburnea) in order to infer the connectivity among gull colonies. We analyzed 343 individuals sampled from 16 localities across the circumpolar breeding range of ivory gulls, from northern Russia to the Canadian Arctic. To explore the roles of natal and breeding dispersal, we developed a population genetic model to relate dispersal behavior to the observed genetic structure of worldwide ivory gull populations. Our key finding is the striking genetic homogeneity of ivory gulls across their entire distribution range. The lack of population genetic structure found among colonies, in tandem with independent evidence of movement among colonies, suggests that ongoing effective dispersal is occurring across the Arctic Region. Our results contradict the dispersal patterns generally observed in seabirds where species movement capabilities are often not indicative of dispersal patterns. Model predictions show how natal and breeding dispersal may combine to shape the genetic homogeneity among ivory gull colonies separated by up to 2800 km. Although field data will be key to determine the role of dispersal for the demography of local colonies and refine the respective impacts of natal versus breeding dispersal, conservation planning needs to consider ivory gulls as a genetically homogeneous, Arctic-wide metapopulation effectively connected through dispersal.     

Behavioural plasticity in nest-site selection of a colonial seabird in response to an invasive carnivore

Non-native invasive species are one of the most serious threats to biodiversity and are considered the leading cause of extinction of several bird taxa, including seabirds. Introduced American mink (Neovison vison) have caused devastating effects on island populations of several colonial seabird species. In this study, we investigated the direct and indirect effects of mink on population dynamics and reproductive success of European shags (Phalacrocorax aristotelis) breeding at Illas Cíes, one of the most important colonies of the species in Southern Europe. A severe episode of mink predation on adult shags occurred in the year when mink arrived in the breeding colonies, though the number of shags killed dropped abruptly in subsequent years. We found that, after the arrival of mink, shags moved to nest-sites that afforded greater protection from carnivores. This shift caused a substantial reduction in mortality by predation, but probably entailed a cost in terms of their reproductive success because sites with lower levels of predation risk showed a higher risk of egg loss by nest flooding due to poorer drainage. Our study highlights that behavioural plasticity may allow shags to cope with invasive predators.     

Increased fluctuating asymmetry in the damselfly Coenagrion puella is correlated with ectoparasitic water mites: implications for fluctuating asymmetry theory

The influence of ectoparasitic water mite larvae (Arrenurus) on the fluctuating asymmetry (FA) of forewing length and cell number in the foreweings of the damselfly Coenagrion puella has been investigated. We show a significant correlation between the FA of forewing length and the mite load. Most explanations for increases in FA implicate environmental stress combined with the inability of the genome to stabilize the phenotype. In contrast, our results demonstrate that FA could be the result of a very short-term impact during ontogenesis, due to chance parasitism.     

Testing life history predictions in a long-lived seabird: a population matrix approach with improved parameter estimation

Life history theory and associated empirical generalizations predict that population growth rate (λ) in long-lived animals should be most sensitive to adult survival; the rates to which λ is most sensitive should be those with the smallest temporal variances; and stochastic environmental events should most affect the rates to which λ is least sensitive. To date, most analyses attempting to examine these predictions have been inadequate, their validity being called into question by problems in estimating parameters, problems in estimating the variability of parameters, and problems in measuring population sensitivities to parameters. We use improved methodologies in these three areas and test these life-history predictions in a population of red-tailed tropicbirds ( Phaethon rubricauda ). We support our first prediction that λ is most sensitive to survival rates. However the support for the second prediction that these rates have the smallest temporal variance was equivocal. Previous support for the second prediction may be an artifact of a high survival estimate near the upper boundary of 1 and not a result of natural selection canalizing variances alone. We did not support our third prediction that effects of environmental stochasticity (El Niño) would most likely be detected in vital rates to which λ was least sensitive and which are thought to have high temporal variances. Comparative data-sets on other seabirds, within and among orders, and in other locations, are needed to understand these environmental effects.     

Influence of environmental variability on breeding effort in a long-lived seabird, the yellow-nosed albatross

The provisioning parameters, breeding success, adult mass, andsurvival of yellow-nosed albatrosses were studied over 7 successiveyears at Amsterdam Island, southern Indian Ocean. We examinedthe ability of this long-lived seabird to adjust its breedingeffort under different environmental conditions and the fitnessconsequences in terms of survival and quality of offspringproduced. Provisioning rate and adult mass varied extensivelybetween years, and the lowest and highest values were associatedwith sea surface temperature anomalies. When waters aroundthe island were colder, adults were in good condition and broughtlarge meals at short intervals, whereas warmer waters resultedin lower provisioning rates, lower adult mass, and lighter chicksat fledging. Adult survival and fledging success were not affectedby sea surface temperature anomalies. Yellow-nosed albatrossesappear to be unable to adjust their breeding effort every season,and their differential breeding investment probably primarilyreflects different levels of food availability. Yellow-nosedalbatrosses are able to regulate their provisioning behavioraccording to the nutritional status of their chick only whenconditions are favorable. Birds appear to invest primarilyin their own future maintenance rather than in provisioning.They have a wide safety margin in body mass that limits mortalityrisks during good years as well as during poor years. However,during unfavorable seasons adults continue to provision chicksthat have a poor prospect of survival to breeding, withoutadditional survival costs for the parents. Favorable seasonstherefore have a high value in terms of fitness because ofthe high quality of the chick produced. We suggest that understandinghow long-lived animals optimize their provisioning behaviorand lifetime reproduction can only be achieved through studiesencompassing several contrasted seasons.     

Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird

Exposure to stressors early in life is associated with faster ageing and reduced longevity. One important mechanism that could underlie these late life effects is increased telomere loss. Telomere length in early post-natal life is an important predictor of subsequent lifespan, but the factors underpinning its variability are poorly understood. Recent human studies have linked stress exposure to increased telomere loss. These studies have of necessity been non-experimental and are consequently subjected to several confounding factors; also, being based on leucocyte populations, where cell composition is variable and some telomere restoration can occur, the extent to which these effects extend beyond the immune system has been questioned. In this study, we experimentally manipulated stress exposure early in post-natal life in nestling European shags (Phalacrocorax aristotelis) in the wild and examined the effect on telomere length in erythrocytes. Our results show that greater stress exposure during early post-natal life increases telomere loss at this life-history stage, and that such an effect is not confined to immune cells. The delayed effects of increased telomere attrition in early life could therefore give rise to a ‘time bomb’ that reduces longevity in the absence of any obvious phenotypic consequences early in life.     

Carotenoids and egg quality in the lesser blackbacked gull Larus fuscus: a supplemental feeding study of maternal effects.

Egg quality is a phenotype of, and can profoundly influence fitness in, both mother and offspring. However, the physiological mechanisms that underlie this maternal effect are poorly understood. Carotenoids are hypothesized to enhance antioxidant activity and immune function, and are responsible for the pigmentation of egg yolk. The proximate basis and consequences of this maternal investment, however, have not previously been studied in wild birds. In this supplemental feeding study of lesser black-backed gulls, Larus fuscus, carotenoid-fed females are shown to have increased integument pigmentation, higher plasma concentrations of carotenoids and antioxidant activity, and lower plasma concentrations of immunoglobulins (Igs) in comparison with controls. In turn, carotenoid-fed females produced eggs containing high carotenoid but low Ig concentrations (i.e. passive immunity), whereas control females produced eggs containing low carotenoid but high Ig concentrations. Within-clutch patterns of these resources varied over the laying sequence in a similar manner in both carotenoid-fed and control nests. Our results suggest that carotenoids could be one resource responsible for egg quality maternal effects in birds. We discuss the possible implications of carotenoid-mediated effects on phenotype for fitness in mothers and their offspring.