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.


Airplane-based abundance and distribution of seabirds off western iberia – monitoring towards conservation

Fernandes, H.A., 2021. Airplane-based abundance and distribution of seabirds off western Iberia; monitoring towards conservation (Doctoral dissertation, Universidade de Vigo).

In this thesis, multi-annual seabird distribution and abundance were investigated for the first time in WIW using aerial surveys. Each seabird distribution and abundance estimates were presented with the corresponding coefficient of variation (CV) and 95% confidence interval (CI) calculations. MaxEnt software was used to compute seasonal and inter-annual Habitat Suitability models for the Balearic Shearwater and the Northern Gannet. The predicted species distribution was based on occurrence probability in relation to habitat suitability. The use of models with different sets of environmental variables are particularly important in the marine environment because variability in ocean conditions may lead to identifiable species distribution changes (Becker et al. 2017). This modelling approach proved to be effective in determining areas of high and low use by the target species. These data are crucial to policy makers and stakeholders involved in conservation planning, particularly when defining marine protected areas (including SPAs) and threat mitigation measures.

In comparison to vessel platforms, airplane surveys are more cost-effective, use lower effort time and produce a lower responsive effect on seabirds. Data collected in airplane surveys allow estimating absolute and relative abundances and associated errors. Data also allow establishing temporal trends and they can be used to model species distribution. If a double platform is used, airplane surveys reduce the number of animals that are not detected on the line or have evasive responses. However, the availability of suitable platforms for aerial surveys is low, observers must be trained and experienced and the identification of similar species (e.g., Storm-petrels, some Larids and Shearwaters) is difficult. Also, there may be problems in estimating angles to sightings in high-density areas and in collecting additional oceanographic or climatic data. For less common species, there is a risk of high variability in the error associated with sampling, which can hamper the detection of small fluctuations. Overall, line transect aerial surveys proved to be a time and cost-effective method allowing for robust seabird abundance and density estimates across a large study area.

The information collected in this thesis contributed to understand the distribution and abundance of the target species, being necessary for EU member states, such as Portugal and Spain, so that they can meet the European Marine Framework Strategy Directive and the Birds Directive. Furthermore, this information can help decision-makers designate or review proposed marine protection areas. In this study it was also possible to estimate Balearic Shearwater and Northern Gannet PBR in relation to bycatch. Areas of higher bycatch risk were mapped and results emphasised that Balearic Shearwaters bycatch mortality was above the PBR threshold (mostly due to set nets in the Polyvalent fleet). Northern Gannet bycatch mortality was at the PBR limit (mostly due to the Longliner and Polyvalent fleets). These data highlighted the necessity for implementation of mitigation measures to reduce seabird bycatch in fisheries, defined and enforced by European or national governmental agencies, to particularly with focus on the critically endangered Balearic Shearwater.



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..


Seabird abundance and distribution off western Iberian waters estimated through aerial surveys

Araujo, H., Correia-Rodrigues, P., Bastos-Santos, J., Ferreira, M., Pereira, A.T., Martinez-Cedeira, J., Vingada, J. and Eira, C., 2022. Seabird abundance and distribution off western Iberian waters estimated through aerial surveys. Marine Ornithology, 50, pp.71-80.

Western Iberian waters are important migratory flyways, stopover sites, and wintering areas for several of the world’s seabird species. To describe seabird species composition, distribution, and abundance in these waters, we performed six aerial surveys in September and/ or October of each year, 2010–2015, covering 74840 km2. Using line-transect methodology, 27396 seabird sightings from 17 taxonomic groups were recorded along 10496.3 nautical miles (19 433 km). Using the program “Distance,” annual and overall abundance estimates were obtained for nine taxonomic groups: Balearic Shearwater Puffinus mauretanicus, Great Shearwater Ardenna gravis, Cory’s Shearwater Calonectris borealis, shearwaters, Northern Gannet Morus bassanus, Sabine’s Gull Xema sabini, Great Skua Stercorarius skua, storm petrels, and Red Phalarope Phalaropus fulicarius. For the six-year period, Northern Gannet was the most abundant species (89 630 individuals, coefficient of variation [CV] = 6.28%), followed by Cory’s Shearwater (25 044 individuals, CV = 7.56%) and Balearic Shearwater (13 632 individuals, CV = 20.81%). The remaining taxonomic groups exhibited variable abundances. Results confirm that the study area is important to several seabird species, providing baseline estimates to inform conservation policies and instruments, such as the Birds Directive and the Marine Strategy Framework Directive.


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.


Global deposition of potentially toxic metals via faecal material in seabird colonies

De La Peña-Lastra, S., Pérez-Alberti, A., Ferreira, T.O., Huerta-Díaz, M.Á. and Otero, X.L., 2022. Global deposition of potentially toxic metals via faecal material in seabird colonies. Scientific Reports, 12, p.22392.

Seabirds are known to play an important role in the geochemical cycling of macronutrients; however, their role in cycling elements of environmental interest has not been investigated. Guano is an important source of marine-derived nutrients and trace metals in seabird nesting areas, but most of the available information on this topic is derived from local studies. In the present study, we used a bioenergetic model to estimate the amounts of cadmium (Cd), mercury (Hg) and lead (Pb) that are deposited via faecal material in seabird colonies worldwide. The findings showed that the seabirds excreted 39.3 Mg (Mg = metric ton or 1000 kg) of Cd, 35.7 Mg of Hg and 27.2 Mg of Pb annually. These amounts are of the same order of magnitude as those reported for other fluxes considered in the geochemical cycling of these elements (e.g. sea-salt spray, cement production, soil loss to oceans). Most of the deposition occurs in circumpolar zones in both hemispheres and, interestingly, high proportions of the metals in the excrements occur in geochemically labile forms, which can be easily leached into coastal waters and assimilated by marine organisms.