Gut microbiome and telomere length in gull hatchlings

Velando, A., Noguera, J.C., Aira, M. and Domínguez, J., 2021. Gut microbiome and telomere length in gull hatchlings. Biology Letters, 17(10), p.20210398.

In many animals, recent evidence indicates that the gut microbiome may be acquired during early development, with possible consequences on newborns’ health. Thus, it has been hypothesized that a healthy microbiome protects telomeres and genomic integrity against cellular stress. However, the link between the early acquired microbiome and telomere dynamics has not hitherto been investigated. In birds, this link may also be potentially modulated by the transfer of maternal glucocorticoids, since these substances dysregulate microbiome composition during postnatal development. Here, we examined the effect of the interplay between the microbiome and stress hormones on the telomere length of yellow-legged gull hatchlings by using a field experiment in which we manipulated the corticosterone content in eggs. We found that the hatchling telomere length was related to microbiome composition, but this relationship was not affected by the corticosterone treatment. Hatchlings with a microbiome dominated by potential commensal bacteria (i.e. Catellicoccus and Cetobacterium) had larger telomeres, suggesting that an early establishment of the species-specific microbiome during development may have important consequences on offspring health and survival.


Distribution and ten-year temporal trends (2009–2018) of perfluoroalkyl substances in gull eggs from Spanish breeding colonies

Colomer-Vidal, P., Bertolero, A., Alcaraz, C., Garreta-Lara, E., Santos, F. J., & Lacorte, S. (2022). Distribution and ten-year temporal trends (2009–2018) of perfluoroalkyl substances in gull eggs from Spanish breeding colonies. Environmental Pollution, 293, 118555.

Gull eggs are excellent bioindicators of environmental pollution as reflect the contamination levels of coastal areas, especially of persistent and bioacumulative compounds such as perfluoroalkyl substances (PFAS). This study aims to evaluate the geographical distribution and 10-year temporal trends (2009–2018) of 17 PFAS in eggs of two gull species (Larus michahellis and Larus audouinii) from 5 main Spanish colonies. ∑PFAS ranged from 13.7 ± 5.9 to 164 ± 17 ng g−1 wet weight and higher concentrations were observed in L. audouinii than in L. michahellis. Perfluorooctane sulfonate (PFOS) was the predominant compound in all samples, followed by perfluoroundecanoic acid (PFUnA) and perfluorotridecanoic acid (PFTriDA). Perfluorododecanoic acid (PFDoA), perfluorodecanoic acid (PFDA) and perfluorooctanoic acid (PFNA) were also found in all studied areas but at lower concentrations, while perfluorooctanoic acid (PFOA) was only detected in the Medes Islands. Principal Component Analysis revealed the co-occurrence of the 6 detected PFAS, and differentiated samples from Ebro Delta and Medes Islands, both located in the North-Eastern Mediterranean Sea, with high contribution of all PFAS, from Chafarinas and Atlantic Islands with lower concentration levels and variability. Also, different patterns were observed among colonies, suggesting the fish-based diet plays an important role in PFAS bioaccumulation. In all colonies, except for the Medes Islands, ∑PFAS decreased through the 10-year study period, with PFOS, PFUnA, and PFTriDA showing a significant concentration reduction in a colony-specific manner. This study demonstrates the usefulness and importance of continuous systematic long-term monitoring to determine the geographical distribution and temporal variations of PFAS in marine protected areas using gull eggs as bioindicators of environmental pollution.


Faeces of marine birds and mammals as substrates for microbial plankton communities

Alba-González, P., Álvarez-Salgado, X.A., Cobelo-García, A., Kaal, J. and Teira, E., 2022. Faeces of marine birds and mammals as substrates for microbial plankton communities. Marine Environmental Research, 174, p.105560.

The chemical composition of the seawater soluble fraction (WSF) of yellow-legged gulls and harbour seal faeces and their impact on microbial plankton communities from an eutrophic coastal area have been tested. After characterisation of the C:N:P stoichiometry, trace metals content and organic molecular composition of the faeces, significant differences between species have been observed in all parameters. Seagull faeces present about three times larger N content than seal faeces and are also richer in trace elements except for Cu and Zn. Organic nitrogen in seagull faeces is dominated by uric acid, while the proteins are the main N source in seal faeces. It is remarkable that seagull faeces are five times more soluble in seawater than seal faeces and present a much higher N content (48.0 versus 3.5 mg N in the WSF per gram of dry faeces), >85% of which as dissolved organic nitrogen, with C:N molar ratios of 2.4 and 13 for seagull and seal faeces, respectively. Based on this contrasting N content, large differences were expected in their impact on microbial populations. To test this hypothesis, a 3-day microcosm incubation experiment was performed, in which coastal seawater was amended with realistic concentrations of the WSF of seagull or seal faeces. A significant and similar increase in bacterial biomass occurred in response to both treatments. In the case of phytoplankton, the impact of the treatment with seagull faeces was significantly larger that the effect of the treatment with seal faeces. Our data suggest that the distinct competitive abilities of phytoplankton and bacteria largely influence the potential impact of distinct animal faeces on primary productivity in coastal ecosystems. Impacts on the microbial plankton communities do not affect only this trophic level, but the whole trophic chain, contributing to nutrient recycling in coastal areas where large populations of these species are settled.


The Rapid Effects of Yellow-Legged Gull (Larus michahellis) Colony on Dune Habitats and Plant Landscape in the Atlantic Islands National Park (NW Spain)

Peña-Lastra, S.D.L., Torre, F., Carballeira, R., Santiso, M.J., Pérez-Alberti, A. and Otero, X.L., 2022. The Rapid Effects of Yellow-Legged Gull (Larus michahellis) Colony on Dune Habitats and Plant Landscape in the Atlantic Islands National Park (NW Spain). Land, 11(2), p.258.


The Atlantic Islands of Galicia Maritime/Terrestrial National Park hosts one of the largest breeding colonies of yellow-legged gull (Larus michahellis) in the world. In 2002, a new yellow-legged gull breeding colony was established on the Punta Muxieiro dune complex, which also harbors rare and threatened plant species and habitat types of community interest according to Directive 92/43/EEC. This study assesses the effect of this colony on two habitats of community interest: white dunes and grey dunes. For this purpose, plant cover and soil properties, composition, and nutrient content were monitored in plots with different gull densities. Moreover, historic aerial images were compiled to observe changes in the plant landscape of the dune system. The results showed that, despite the recentness of the occupation of the dune system by yellow-legged gull species, significant changes in acidic–alkaline processes and nutrient availability were already observed in soils. Soils in plots with higher gull density showed more acidic pH values and a higher content of the most labile N and P fractions. Moreover, a decrease in plant cover and number of species was also demonstrated in plots with higher gull densities. Finally, the presence of ruderal and alien species such as Urtica membranacea and Parietaria judaica was also observed..


Heavy metals and metalloid levels in the tissues of yellow-legged gulls (Larus michahellis) from Spain: sex, age, and geographical location differences

Vizuete, J., Hernández-Moreno, D., López-Beceiro, A., Fidalgo, L.E., Soler, F., Pérez-López, M. and Míguez-Santiyán, M.P., 2022. Heavy metals and metalloid levels in the tissues of yellow-legged gulls (Larus michahellis) from Spain: sex, age, and geographical location differences. Environmental Science and Pollution Research, 29(36), pp.54292-54308.

Mercury (Hg), cadmium (Cd), lead (Pb), selenium (Se), and arsenic (As) were measured in liver, kidney, and feathers of adult, juvenile, and chick seagulls (Larus michahellis) collected from the northwest of Spain. Age, sex, and the geographical location of samples were considered variables that can influence metal bioaccumulation, for which concentrations were determined by means of ICP-MS. The mean concentrations (dry weight) found in seagulls were 7.01 ± 0.37 mg Hg/kg, 22.82 ± 2.83 mg Cd/kg, 7.36 ± 1.36 mg Pb/kg, 18.64 ± 0.63 mg Se/kg, and 10.64 ± 0.59 mg As/kg. Regarding the different factors analyzed, Hg was the only metal showing sex-related differences, being significantly higher (p < 0.05) the concentrations found in feathers of males (1.26 ± 0.12 mg/kg) than those in females (0.99 ± 0.11 mg/kg). A highly significant (p < 0.01) increase in levels of some metals was found in liver related to the increase of age: Hg (adults (A) 3.33 ± 0.22 mg/kg vs chicks (C) 1.76 ± 0.28 mg/kg), Cd (A 4.74 ± 0.62 mg/kg vs C 1.79 ± 0.2), Pb (A 0.65 ± 0.12 mg/kg vs juveniles 0.4 ± 0.11 mg/kg), and Se (A 7.56 ± 0.43 mg/kg vs C 5.24 ± 0.53 mg/kg). Positive correlations between Cd-Hg and Se–Hg were found in liver (p < 0.001), kidney (p < 0.001), and feathers (p < 0.05 and p < 0.001, respectively). The associations found may reflect antagonistic interactions between Se and Cd on Hg toxicity. The results suggest that L. michahellis can reveal local contamination around the foraging and breeding sites and can be a very useful monitoring instrument for assessing heavy metal contamination and sentinel species of environmental health..


Light received by embryos promotes postnatal junior phenotypes in a seabird

Ruiz-Raya, F., Noguera, J.C. and Velando, A., 2022. Light received by embryos promotes postnatal junior phenotypes in a seabird. Behavioral Ecology, 33(6), pp.1047-1057.

Light is a salient and variable ecological factor that can impact developmental trajectories of vertebrate embryos, yet whether prenatal light environment can act as an anticipatory cue preparing organisms to cope with postnatal conditions is still unclear. In asynchronous birds, last-laid eggs are particularly exposed to sunlight as parental incubation behavior becomes intermittent after the hatching of senior chicks. Here, we explore whether natural variations in prenatal light exposure shape the distinctive phenotype showed by last-hatched chicks of a semi-precocial seabird, the yellow-legged gull (Larus michahellis), potentially preparing them to cope with the postnatal competitive context. To do this, we manipulated the amount of light received by last-laid eggs (within a natural range) during last stages of embryonic development. Prenatal exposure to light cues promoted the development of the resilient “junior phenotype” exhibited by last-hatched gull chicks, characterized by accelerated hatching, increased begging behavior and a slower growth rate. These developmental and behavioral adjustments were accompanied by down-regulation of genes involved in metabolism and development regulation (SOD2 and TRalpha), as well as changes in the HPA-axis functioning (lower baseline corticosterone and robust adrenocortical response). Junior chicks exposed to light cues during the embryonic development showed longer telomeres during the early postnatal period, suggesting that light-induced adjustments could allow them to buffer the competitive disadvantages associated with hatching asynchrony. Our study provides evidence that postnatal junior phenotypes are, at least in part, prenatally shaped by light cues that act during a critical temporal window of developmental sensitivity.


Maternal testosterone affects offspring telomerase activity in a long-lived seabird

Noguera, J.C. and Velando, A., 2022. Maternal testosterone affects offspring telomerase activity in a long‐lived seabird. Ecology and Evolution, 12(9), p.e9281.

Androgens are a group of steroid hormones that have long been proposed as a mechanism underpinning intergenerational plasticity. In birds, maternally allocated egg testosterone, one of the main androgens in vertebrates, affects a wide variety of offspring phenotypic traits but the mechanisms underlying this form of intergenerational plasticity are not yet well understood. Recent in vitro and animal model studies have shown that telomerase expression and activity are important targets of androgen signaling. The telomerase enzyme is known for its repair function on telomeres, the DNA–protein complexes at the ends of chromosomes that are involved in genomic integrity and cell aging. However, the role of maternal testosterone in influencing offspring telomerase levels in natural populations and its consequences on telomere length and potentially on offspring development is still unknown. Here, by experimentally modifying the level of egg testosterone in a natural population of yellow-legged gull (Larus michahellis), we show that chicks hatched from testosterone-treated eggs had higher average levels of telomerase and faster growth than controls during the first week of life. While testosterone-treated chicks also tended to have longer telomeres than controls at hatching this difference disappeared by day 6 of age. Overall, our results suggest that maternal testosterone may have a potential adaptive value by promoting offspring growth and presumably telomerase levels, as this enzyme plays other important physiological functions (e.g., stress resistance, cell signaling, or tissue genesis) besides telomere lengthening. Nonetheless, our knowledge of the potential adaptive function of telomerase in natural populations is scarce and so the potential pathways linking maternal hormones, offspring telomerase, and fitness should be further investigated.


Soil eutrophication in seabird colonies affects cell wall composition: Implications for the conservation of rare plant species

Otero, X.L., Fernández-Balado, C., Ferreira, T.O., Pérez-Alberti, A. and Revilla, G., 2021. Soil eutrophication in seabird colonies affects cell wall composition: Implications for the conservation of rare plant species. Marine Pollution Bulletin, 168, p.112469.

Seabird colonies exert a strong influence on coastal ecosystems, increasing soil nitrogen bioavailability and modifying plant communities. Previous studies have evidenced that increased N in soils leads to changes in plant cell wall composition; however, this effect has not been assessed in seabird colonies. The main objective of this study was to determine the influence of seabird colonies on nitrogen, cellulose and lignin content in cell walls. For this purpose, analyses were performed on droppings, soils and three native plant species (Armeria pubigera, Armeria pungens and Corema album) growing in yellow-legged gull colonies. The results showed that N excreted by yellow-legged gull is assimilated by plants, increases N content in plant tissues and reduces cellulose and lignin synthesis, therefore potentially altering plant resistance against phytoparasites.


Influence of fisheries on the spatio-temporal feeding ecology of gulls along the western Iberian coast

Calado, J.G., Veríssimo, S.N., Paiva, V.H., Ramos, R., Vaz, P.T., Matos, D., Pereira, J., Lopes, C., Oliveira, N., Quaresma, A. and Ceia, F.R., 2021. Influence of fisheries on the spatio-temporal feeding ecology of gulls along the western Iberian coast. Marine Ecology Progress Series, 661, pp.187-201

Gulls are highly opportunistic seabirds, and the exploitation of fishery discards has led to many population increases worldwide. We investigated the importance of fish in the diet of yellow-legged Larus michahellis and Audouin’s gulls L. audouinii and assessed the influence of fishery discards on their feeding ecology. We collected pellets from 4 islands along the western Iberian coast during pre-breeding, breeding, and post-breeding seasons from 2014 to 2018. Stable isotopes (from adult blood, and chick and adult feathers) were used to investigate spatial, seasonal, and inter-annual differences in their feeding ecology. We used pellet, stable isotope (δ15N, δ13C, and δ34S), and biochemical (triglycerides, uric acid, total protein, and carotenoids in adult plasma) analyses to investigate their relationships with fish landings across the annual cycle. Results revealed that the fish species consumed by gulls matched those landed by local fisheries on all study islands, and there was a positive association of pelagic and demersal fish diets with fish landing quantities for 2 islands. δ34S values suggest different self-feeding and chick-provisioning strategies in relation to fisheries. δ15N values exhibited strong negative correlations with fish landings, and triglycerides were positively correlated with pelagic but not with demersal fish landing quantities, suggesting that gulls fed more on lower trophic level and higher energetic content pelagic fish than on demersal fish. Overall, our results based on several techniques suggest that gull feeding ecology was linked to fishery discards, which in view of the new EU landing obligation may have major implications for both gull populations across Europe.

Seabird colonies as the main source of nutrients for the coastal ecosystems in the Atlantic Islands of Galicia National Park (NW Spain)

De La Peña-Lastra, S., Pérez-Alberti, A. and Otero, X.L., 2021. Seabird colonies as the main source of nutrients for the coastal ecosystems in the Atlantic Islands of Galicia National Park (NW Spain). Chemosphere, 275, p.130077.

Seabirds form large colonies during the reproductive period, producing substantial changes in coastal ecosystems. The present study quantifies the amount of N and P deposited in colonies of yellow-legged gull (Larus michahellis) in the Atlantic Islands of Galicia National Park (AINP). Based on the composition of droppings, the amount of total N (TN), total P (TP) and bioavailable P (Pbio) deposited directly on the area occupied by the colony was determined. In addition, the amount of NH3 released into the atmosphere was also estimated by applying a bioenergetic model. The results indicated that 5.35 t total N, 3.35 t total P and 1.24 t bioavailable P are deposited in the colony annually. The archipelagos that received the greatest amount of nutrients were the Cíes Islands (2.37 t TN y−1, 1.48 t TP y−1, 0.55 t Pbio y−1), Sálvora (1.94 t TN y−1, 1.22 t TP y−1, 0.55 t Pbio y−1) and Ons (1.04 t TN y−1, 0.65 TP y−1, 0.24 t Pbio y−1). Rainwater from the colonies showed higher values of nutrients than in the control plot, possibly also due to gull influence. Therefore, the yellow-legged gull colony seems to be the most important source of nutrients at a local level, exerting a clear influence on the N and P cycles in this National Park. Another aspect worth taking into consideration is that increased N and P bioavailability may have a negative effect on the conservation of rare or threatened habitats and species by promoting the expansion of non-native ruderal species.