A spatial analysis of urban gulls contribution to the potential spread of zoonotic and antibiotic-resistant bacteria.

Wildlife human interactions within cities are becoming more common with consequences for pathogen transmission and human health. Large gulls are opportunistic feeders, adapted to coexist with humans in urban environments, and are potential vectors for spread and transmission of pathogens, including antimicrobial-resistant bacteria. We investigated the potential role that urban gulls play in the spread and dispersal of these bacteria. We analysed 129 faecal swabs from yellow-legged gulls (Larus michahellis) of different ages (56 adults and 73 immatures) during the breeding period from three years in the highly populated city of Barcelona (northeastern Spain). Thirteen individuals tested positive for the pathogenic bacteria (Escherichia coli, Listeria monocytogenes, Campylobacter jejuni), including antibiotic-resistant strains. We modelled the potential spatial spread of pathogens using the GPS trajectories of 58 yellow-legged gulls (23 adults, 35 immature individuals), which included the thirteen individuals that tested positive for pathogenic bacteria. By overlapping the spatially explicit pathogen dispersal maps with the distribution of urban installations sensitive at risk of possible pathogen spillover (e.g. elder and medical centres, markets, food industries, kindergartens, or public water sources), we identified potential areas at risk of pathogen spillover. Pathogens may be potentially spread to municipalities beyond Barcelona city borders. The results revealed that immature gulls dispersed pathogens over larger areas than adults (maximum dispersal distances of 167 km versus 53.2 km, respectively). Recreational urban water sources were the most sensitive habitats visited by GPS-tagged gulls that tested positive, followed by schools. Combining GPS movement data with pathogen analytics allows spatially explicit maps to be generated using a One Health approach that can help urban and public health management within large cities, such as Barcelona, and identify areas used by humans that are sensitive to pathogen spillover from gulls.

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

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.

Gulls living in cities as overlooked seed dispersers within and outside urban environments.

The yellow-legged gull is an opportunistic and generalist bird that has colonised urban areas, where it has found very favourable trophic resources but also causes disturbance to humans and damage to infrastructure. Here, we investigated the potential role that gulls play in the dispersal of plants in Barcelona, a highly populated city of north-eastern Spain. We analysed the stomach contents of 145 chicks collected in urban nests and reported the presence of seeds of 27 plant taxa. We then developed a plant dispersal model based on the movements of 20 GPS-tracked yellow-legged gulls breeding in the city of Barcelona. We estimated seed dispersal distances, seed shadows and percentage of seeds reaching habitats suitable for seeds regurgitated in pellets and those excreted in faeces. Seven of the 27 plant taxa found in the stomachs were alien taxa to Spain. Average dispersal distances of plant seeds by gulls were around 700 m, but maximum dispersal distances reached up to 35 km. Dispersal distances and seed spatial patterns did not differ between faeces and pellet models, as most strongly depended on gull movements. About 95% of the seeds were dispersed within urban environments and between 20 and 30% reached suitable habitats for seed deposition (urban woodlands, green urban parks and urban grasslands). Urban gulls frequently dispersed seeds (including alien species) within urban habitats, both via direct consumption or via secondary dispersal after consuming granivorous birds that had ingested the seeds, such as pigeons or parakeets. Urban planning for Barcelona is based on native plant species, and thus, special attention should be paid to alien plants dispersed by birds, which could pose a risk to native biodiversity in urban ecosystems.

Sex determination based on morphometric measurements in yellow-legged gulls (Larus michahellis) around Istanbul.

BACKGROUND: Yellow-legged gulls (Larus michahellis), commonly found in Istanbul and their surroundings, have a monomorphic plumage, like other gull species. For this reason, sex determination cannot be made externally. In this study, a total of 60 adult Yellow-legged gulls, 33 males, and 27 females, collected from the coastal areas of Istanbul, were examined. Discriminating functions were developed to classify males and females using birds that were previously sexed by DNA analysis and abdominal dissection. RESULTS: Head length and bill depth were selected to build the discriminant function by the stepwise analysis. The function classified male gulls with an accuracy of 97.0% and females with an accuracy of 92.6%. Head length alone is the most accurate predictor in terms of the percentage of correct sex determination (90.9% for males, 92.6% for females). CONCLUSIONS: Functions that can easily determine sexual dimorphism for the population of Larus michahellis gulls around Istanbul have been put forward for the first time.

Prenatal exposure to triclosan induced brain telomere shortening in a wild bird species.

Exposure to the antimicrobial agent Triclosan (TCS) induces oxidative stress in diverse organisms, including birds. However, whether TCS-induced oxidative stress effectively translates into detrimental effects is still unclear. The present study examined whether prenatal TCS exposure induces oxidative stress and telomere shortening in the brain and the liver of near-term embryos of the yellow-legged gull (Larus michahellis). Prenatal TCS exposure caused a significant overproduction of reactive oxygen species (ROS) in the brain, but no oxidative damage occurred. Telomeres of TCS-exposed embryos had brain telomeres 30 % shorter compared to controls, probably because the relatively modest antioxidant defenses of this organ during prenatal development cannot counteract the impact of the TCS-induced ROS. No telomere shortening was observed in the liver. Our results demonstrated that prenatal exposure to TCS in wild bird species can modulate the oxidative status and induce telomere shortening in the brain of the yellow-legged gull embryos.

Telomerase activity can mediate the effects of growth on telomeres during post-natal development in a wild bird.

In wild animals, telomere attrition during early development has been linked with several fitness disadvantages throughout life. Telomerase enzyme can elongate telomeres, but it is generally assumed that its activity is suppressed in most somatic tissues upon birth. However, recent evidence suggests that this may not be the case for long-lived bird species. We have therefore investigated whether telomerase activity is maintained during the postnatal growth period in a wild yellow-legged gull (Larus michahellis) population. Our results indicate that telomerase activity is not negligible in the blood cells, but activity levels sharply decline from hatching to fledging following a similar pattern to the reduction observed in telomere length. Our results further suggest that the observed variation in telomere length may be the result of a negative effect of fast growth on telomerase activity, thus providing a new mechanism through which growth rates may affect telomere dynamics and potentially life-history trajectories.

Prevalence and Antimicrobial Resistance of Enteropathogenic Bacteria in Yellow-Legged Gulls (Larus michahellis) in Southern Italy.

Wild birds may host and spread pathogens, integrating the epidemiology of infectious diseases. Particularly, Larus spp. have been described as responsible for the spread of many enteric diseases, primarily because of their large populations at landfill sites. The aim of this study was to examine the role of yellow-legged gulls as a source of enteropathogenic bacteria such as Campylobacter spp., Salmonella spp., Shiga toxin-producing Escherichia coli and Yersinia spp., with particular attention to antibiotic-resistant strains. Enteropathogenic bacteria were isolated from 93/225 yellow-legged gulls examined from April to July, during a four-year period (2016-2019). Specifically, Campylobacter spp. was isolated from 60/225 samples (26.7%), and identified as C. coli (36/60) and as C. jejuni (24/60). Salmonella spp. was isolated from 3/225 samples (1.3%), and identified as Salmonella arizonae. Shiga toxin-producing E. coli were isolated from 30/225 samples (13.3%) samples, and serotyped as E. coli O128 (12/30) O26 (9/30), O157 (6/30) and O11 (3/30); Yersinia spp. was never detected. Isolated strains exhibited multidrug resistance, including vitally important antibiotics for human medicine (i.e., fluoroquinolones, tetracyclines). Our study emphasizes the importance of yellow-legged gulls as potential reservoirs of pathogenic and resistant strains and their involvement in the dissemination of these bacteria across different environments, with resulting public health concerns.

Rhamphotheca as a useful indicator of mercury in seabirds.

The evaluation of mercury (Hg) toxicity in wildlife species has prompted a search for sensitive indicators to accurately measure the body burden of Hg. Despite the extensive use of feathers as an indicator of Hg in birds, they do not appear to be an entirely suitable indicator of the extent of contamination in certain conditions and bird species since Hg levels are influenced by the growth period, timing of the last moult and migration. This research aimed to evaluate rhamphotheca as a potential indicator of environmental Hg concentrations in seabirds. We used culled yellow-legged gulls (Larus michahellis) (n = 20) and determined THg in rhamphotheca and feathers. We distinguished between upper and lower rhamphotheca, and divided each one into 16 equal portions along the culmen to analyse their THg content spatially. In each bird, THg was also determined in primary (P1) and secondary (S8) feathers and compared with rhamphotheca. The median (25th, 75th percentile) rhamphotheca Hg concentration was 13.44 (9.63, 17.46) µg/g, which was twofold higher than in the feathers 7.56 (4.88, 12.89) µg/g. Median THg in rhamphotheca was significantly higher (p < 0.05) in females 15.05 (10.35, 23.04) µg/g than in males 12.34 (8.57, 15.19) µg/g, whereas no differences (p > 0.05) were found in the feathers. No significant differences in Hg levels were found between upper and lower beak mandibles or along either. In contrast, significant differences in Hg concentrations were found between the P1 and S8 feathers (mean, 12.04 vs. 6.04 µg/g). No correlation was found between Hg content in rhamphotheca and feathers. Mercury levels in rhamphotheca exhibited stronger significant relationships with weight (R2 = 0.568), length (R2 = 0.524) and culmen (R2 = 0.347) than the levels in the feathers, which showed no correlation. Overall, our results suggest that rhamphotheca is a suitable tissue indicator for Hg monitoring in gulls; however, further studies are needed to extend our research to other bird species.

Humans shape the year-round distribution and habitat use of an opportunistic scavenger.

Research focused on evaluating how human food subsidies influence the foraging ecology of scavenger species is scarce but essential for elucidating their role in shaping behavioral patterns, population dynamics, and potential impacts on ecosystems. We evaluate the potential role of humans in shaping the year-round distribution and habitat use of individuals from a typical scavenger species, the yellow-legged gull (Larus michahellis), breeding at southwestern Spain. To do this, we combined long-term, nearly continuous GPS-tracking data with spatially explicit information on habitat types and distribution of human facilities, as proxied by satellite imagery of artificial night lights. Overall, individuals were mainly associated with freshwater habitats (mean proportion, 95% CI: 40.6%, 36.9%-44.4%) followed by the marine-related systems (40.3, 37.7%-42.8%), human-related habitats (13.5%, 13.2%-13.8%), and terrestrial systems (5.5%, 4.6%-6.5%). However, these relative contributions to the overall habitat usage largely changed throughout the annual cycle as a likely response to ecological/physiological constraints imposed by varying energy budgets and environmental constraints resulting from fluctuations in the availability of food resources. Moreover, the tight overlap between the year-round spatial distribution of gulls and that of human facilities suggested that the different resources individuals relied on were likely of anthropogenic origin. We therefore provide evidence supporting the high dependence of this species on human-related food resources throughout the annual cycle. Owing to the ability of individuals to disperse and reach transboundary areas of Spain, Portugal, or Morocco, international joint efforts aimed at restricting the availability of human food resources would be required to manage this overabundant species and the associated consequences for biodiversity conservation (e.g., competitive exclusion of co-occurring species) and human interests (e.g., airports or disease transmission).

Reduced telomere length in embryos exposed to predator cues.

It is often assumed that embryos are isolated from external influences, but recent studies indicate that environmental stressors during prenatal stages can exert long-term negative effects on fitness. A potential mechanism by which predation risk may lastingly shape life-history traits and phenotypes is via effects on telomeres. However, whether prenatal exposure to environmental stressors, such as cues of predator presence, affects postnatal telomere length has not hitherto been investigated. Using an experimental design in which we modified the exposure of yellow-legged gull (Larus michahellis) embryos to social cues of predator presence (i.e. alarm calls), we show that prenatally exposed chicks had shorter telomeres after hatching. As young birds with shorter telomere lengths have reduced fledging success, reproductive success and lifespan, the reduced telomere length in the exposed chicks is likely to have long-term fitness consequences. Moreover, our results provide a mechanistic link through which predators may negatively affect population dynamics.

Perinatal variation and covariation of oxidative status and telomere length in yellow-legged gull chicks.

The perinatal period is critical to survival and performance of many organisms. In birds, rapid postnatal growth and sudden exposure to aerial oxygen around hatching markedly affect the chick redox status, with potentially negative consequences on physiology mediated by oxidative stress. In addition, telomere length (TL) undergoes reduction during birds' early life, partly depending on oxidative status. However, relatively few studies have focused specifically on the changes in oxidative status and TL that occur immediately after hatching. In this study of the yellow-legged gull Larus michahellis, we found that chicks undergo a marked increase in plasma total antioxidant capacity and a marked decrease in the concentration of pro-oxidant molecules during the first days after hatching. In addition, TL in erythrocytes decreased by 1 standard deviation over the 4 days post-hatching. Body mass and tarsus length covaried with total antioxidant capacity and concentration of pro-oxidants in a complex way, that partly depended on sex and laying order, suggesting that oxidative status can affect growth. Moreover, TL positively covaried with the concentration of pro-oxidant molecules, possibly because retention of high concentrations of pro-oxidant molecules results from mechanisms of prevention of their negative effects, including reduction in TL. Thus, this study shows that chicks undergo marked variation in oxidative status, which predicts growth and subsequent TL, prompting for more studies of the perinatal changes in the critical post-hatching stages.

Egg Testosterone Differentially Affects Telomere Length in Somatic Tissues of Yellow-Legged Gull Embryos.

Maternal decisions on egg composition have major consequences for offspring. Maternal egg androgens have diverse, often contrasting, effects depending on offspring trait and life stage, suggesting that mothers face trade-offs in egg hormone transfer. However, the effect of egg androgens on embryonic telomere length, which is a major trait potentially affecting performance, has been never investigated. We administered a physiological dose of testosterone (T) to yellow-legged gull (Larus michahellis) eggs and found that, compared to controls, telomere length shortly before hatching was reduced in the liver but unaffected in the brain, heart, and pectoralis muscle. Telomere length varied across somatic tissues, and, independent of egg treatment, it was not correlated between them, suggesting independent telomere dynamics. Thus, we showed for the first time that increased egg T can increase telomere shortening in the embryo and that maternal T allocation strategies may evolve also in response to such effect. Moreover, contrary to observations in adult birds, at the embryonic stage telomere length in one somatic tissue may not reflect telomere length in other body districts.

Embryotoxic effects of in-ovo triclosan injection to the yellow-legged gull.

Triclosan (TCS) is an antimicrobial agent used in diverse personal care products that is considered as an emerging contaminant of both aquatic and terrestrial ecosystems. Although TCS aquatic ecotoxicity is well known, information on the presence and effects on terrestrial organisms is still scarce. This study was aimed at exploring the embryotoxicity of TCS to the yellow-legged gull (Larus michahellis) induced by the in-ovo injection of 150 ng TCS/g egg weight. Effects of TCS on embryo morphological traits (i.e. body mass, tarsus length and head size). Moreover, oxidative and genetic effects were assessed in the embryo liver, by measuring the amount of reactive oxygen species (ROS), the activity of antioxidant (superoxide dismutase and catalase) and detoxifying (glutathione S-transferase - GST) enzymes, the levels of lipid peroxidation and DNA fragmentation. After the injection, the concentration of TCS measured in the yolk of unincubated eggs (159 ±â€¯35 ng/g wet weight, ww) was close to the expected concentration. Triclosan was found in residual yolk (2.9 ±â€¯1.1 ng/g ww), liver (2.3 ±â€¯1.1 ng/g ww) and brain (0.2 ±â€¯0.1 ng/g ww) of embryos soon before hatching. Triclosan did not significantly affect embryo morphological traits, while it increased ROS levels and promoted GST activity, inducing the onset of both oxidative and genetic damage. This study demonstrated, for the first time in a wild euriecious bird species with mixed habits, that TCS can be maternally transferred to developing embryos, representing a potential threat for offspring.

Yolk vitamin E prevents oxidative damage in gull hatchlings.

Oxidative stress experienced during early development can negatively affect diverse life-history traits, and organisms have evolved complex defence systems against its detrimental effects. Bird eggs contain maternally derived exogenous antioxidants that play a major role in embryo protection from oxidative damage, including the negative effects on telomere dynamics. In this study on the yellow-legged gull (Larus michahellis), we manipulated the concentration of vitamin E (VE) in the egg yolk and analysed the consequences on oxidative status markers and telomere length in the hatchlings. This study provides the first experimental evidence that, contrary to the expectation, a physiological increase in yolk VE concentration boosted total antioxidant capacity and reduced the concentration of pro-oxidant molecules in the plasma, but did not reduce telomere attrition or ameliorate oxidative damage to proteins and lipids in the early postnatal period.

Potential toxicity of environmentally relevant perfluorooctane sulfonate (PFOS) concentrations to yellow-legged gull Larus michahellis embryos.

Perfluooctane sulfonate (PFOS) is considered an emerging pollutant because of its wide distribution in both aquatic and terrestrial ecosystems, as well as its potential toxicity to living organisms. Although PFOS environmental levels and the adverse effects on classical model organisms in toxicological studies are well known, including developmental alterations and alteration of oxidative status, its toxicity to free-living species has been seldom investigated. The aim of this study was to assess the potential toxicity of environmental levels of PFOS to yellow-legged gull (Larus michahellis) embryos under field experimental conditions. In a within-clutch experimental design, we injected two PFOS concentrations (100 ng PFOS/g egg weight and 200 ng PFOS/g egg weight) in ovo soon after laying. Eggs were collected when they reached the cracking stage. We investigated the effects of PFOS treatment, laying order and sex on both morphological and biochemical endpoints of embryos. Specifically, we assessed changes in embryo body mass and tarsus length, as well as in liver and brain mass. Moreover, the imbalance of oxidative status was evaluated in both liver and brain from embryos by measuring total antioxidant capacity (TAC) and total oxidant status (TOS), while the levels of protein carbonyl content (PCO) and DNA fragmentation were measured as oxidative and genetic damage endpoints, respectively. The concentrations of PFOS we tested did not significantly alter the morphological endpoints, independently of laying order and sex. Similarly, embryo oxidative status and oxidative and genetic damage were not significantly affected by PFOS in ovo exposure. These findings suggest that current environmental PFOS levels do not affect early development of yellow-legged gull embryos.

Trophic niche width and overlap of two sympatric gulls in the southwestern mediterranean.

The diets of two potential competitor species, Audouin's Larus audouinii and yellow-legged gulls Larus cachinnans, were examined while they bred at the Chafarinas Islands during 1993, 1994, and 1995. Data were collected during two commercial fishing regimes: (1) trawling and purse seine fisheries, and (2) diurnal trawlers only. Since the food supply for the gulls in this area was heavily reliant on the activity of purse seine fisheries, these contrasting situations allowed us to analyze short-term effects, induced by daily changes in food supply, on niche width, dietary shift, and niche overlap between the two species. Overall, both species relied mainly on fish for food, especially Clupeiforms, in the case of Audouin's gull irrespective of the fishing situation, and in the case of the yellow-legged gull, only when purse seine fishing was in operation. When purse seine boats did not operate (food shortage), yellow-legged gulls broadened their niche, consuming equal amounts of all the feeding resources, and they showed a dietary shift toward a greater consumption of prey from refuse tips. In contrast, Audouin's gulls did not change their niche width, but showed a slight dietary shift away from the consumption of epipelagic fish, compensated by an increase in reliance on benthic-mesopelagic resources. Niche overlap was clearly higher on days when both fishing fleets operated, probably because a superabundant food resource facilitates high overlap without affecting coexistence between the two species. Since our study was developed on the basis of daily variations in food supply, and competition effects are to be expected on a longer-term basis, these changes can be seen as the outcome of the coexistence of two species in stable competitive equilibrium.