Larus Michahellis Research Articles

Luc Hoffmann (1923–2016)

Luc Hoffmann (1923–2016)

Contrasting effects of increased yolk testosterone content on development and oxidative status in gull embryos.

Hormone-mediated maternal effects generate variation in offspring phenotype. In birds, maternal egg testosterone (T) exerts differential effects on offspring traits after hatching, suggesting that mothers experience a trade-off between contrasting T effects. However, there is very little information on T pre-natal effects. In the yellow-legged gull (Larus michahellis), we increased yolk T concentration within physiological limits and measured the effects on development and oxidative status of late-stage embryos. T-treated embryos had a larger body size but a smaller brain than controls. Males had a larger brain than females, controlling for overall size. T treatment differentially affected brain mass and total amount of pro-oxidants in the brain depending on laying order. T-treatment effects were not sex dependent. For the first time in the wild, we show contrasting T pre-natal effects on body mass and brain size. Hence, T may enforce trade-offs between different embryonic traits, but also within the same trait during different developmental periods.

Antioxidants and embryo phenotype: is there experimental evidence for strong integration of the antioxidant system?

Organisms have evolved complex defense systems against oxidative stress. Bird eggs contain maternally derived antioxidants that protect embryos from oxidative damage. The antioxidant system components are thought to be integrated, but few studies have analyzed the covariation between antioxidant concentrations, embryo 'oxidative status' and morphology. In addition, no study has tested the effects of experimental change in yolk antioxidant concentration on other antioxidants, on their reciprocal relationships and on their relationships with embryo oxidative status or growth, which are expected if antioxidants defenses are integrated. In yellow-legged gull (Larus michahellis) embryos, we analyzed the covariation between several antioxidants, markers of 'oxidative status' [total antioxidant capacity (TAC), concentration of pro-oxidants (TOS), lipid peroxidation (LPO) and protein carbonylation (PC)] in the yolk, liver and brain, and morphology. Yolk and liver antioxidant concentrations were positively correlated reciprocally and with embryo size, and positively predicted TAC but not oxidative status. TOS and LPO were positively correlated in the liver, while TAC and LPO were negatively correlated in the brain. Weak relationships existed between antioxidants and TOS, PC and LPO. The effects of antioxidants on oxidative status and morphology were non-synergistic. An experimental physiological increase in yolk vitamin E had very weak effects on the relationships between other antioxidants or oxidative status and vitamin E concentration, the concentration of other antioxidants or oxidative status; the covariation between other antioxidants and oxidative status, and relationships between morphology or oxidative status and other antioxidants, challenging the common wisdom of strong functional relationships among antioxidants, at least for embryos in the wild.

Adapting strategies to maintain efficiency during a cull of yellow-legged gulls

Increasing populations of yellow-legged gulls (Larus michahellis) in the Mediterranean have created con? icts with seabird conservation, migrating raptors, and humans. As a mitigation measure, gulls are routinely culled in the region. Previous studies of extended culls show that catch per unit effort declines over time through a combination of population reductions and avoidance behaviors developing within the remaining population. We countered these problems during a 4-year cull of yellow-legged gulls in Gibraltar by matching the type and mode of deployment of o rearms in response to changes in gull distribution and behavior. We found that shotguns were effective when gulls mobbed operators near nesting areas, while ri? es were more effective as gulls became wary and retreated farther from the operators. Changing the type of o rearm enabled us to counter the expected rate of decline in culling efo ciency throughout the project. We were most efo cient in the o rst year of the project, killing gulls at a mean rate of 8.35 birds per man-hour. Although this declined to 4.83 by the third year, the adjustments that we made to the way o rearms were deployed raised it to 6.4 in the fourth year despite a 79% decline in the observed total gull population over this period. We modelled the population data collected using a Leslie Matrix to evaluate the impact of management at the end of the culling period. The population declined at a greater rate than explained by the numbers actually culled, suggesting that the cull resulted in an additional disturbance, which triggered emigration at a rate of 35%, over and above the numbers culled.

VIM-1 carbapenemase-producing Escherichia coli in gulls from southern France.

Acquired carbapenemases currently pose one of the most worrying public health threats related to antimicrobial resistance. A NDM‐1‐producing Salmonella Corvallis was reported in 2013 in a wild raptor. Further research was needed to understand the role of wild birds in the transmission of bacteria resistant to carbapenems. Our aim was to investigate the presence of carbapenem‐resistant Escherichia coli in gulls from southern France. In 2012, we collected 158 cloacal swabs samples from two gull species: yellow‐legged gulls (Larus michahellis) that live in close contact with humans and slender‐billed gulls (Chroicocephalus genei) that feed at sea. We molecularly compared the carbapenem‐resistant bacteria we isolated through culture on selective media with the carbapenem‐susceptible strains sampled from both gull species and from stool samples of humans hospitalized in the study area. The genes coding for carbapenemases were tested by multiplex PCR. We isolated 22 carbapenem‐resistant E. coli strains from yellow‐legged gulls while none were isolated from slender‐billed gulls. All carbapenem‐resistant isolates were positive for bla VIM ‐1 gene. VIM‐1‐producing E. coli were closely related to carbapenem‐susceptible strains isolated from the two gull species but also to human strains. Our results are alarming enough to make it urgently necessary to determine the contamination source of the bacteria we identified. More generally, our work highlights the need to develop more bridges between studies focusing on wildlife and humans in order to improve our knowledge of resistant bacteria transmission routes.

Prevalence of Extended-Spectrum-β-Lactamase- and/or Carbapenemase-Producing Escherichia coli Isolated from Yellow-Legged Gulls from Barcelona, Spain.

Seventy-two (54.5%) out of 132 fecal samples from a group of yellow-legged gulls in Barcelona, Spain, were positive for Escherichia coli producing either extended-spectrum β-lactamases (ESBL) (51.5%), carbapenemase (1.5%), or cephamycinase (1.5%). The isolation of two carbapenemase-producing E. coli strains is a matter of concern.

Yellow-legged Gull Larus michahellis captures and drowns a Feral Pigeon Columba livia

A Yellow-legged Gull catching a Feral Pigeon, flies to a nearby small lake and kills him drowning. This behaviour can be explained or with higher cognitive ability, related with the use of innovative methods, or with a generalist behaviour that offers the opportunity to use new techniques.

Opportunistic fungal pathogen Candida glabrata circulates between humans and yellow-legged gulls.

The opportunistic pathogenic yeast Candida glabrata is a component of the mycobiota of both humans and yellow-legged gulls that is prone to develop fluconazole resistance. Whether gulls are a reservoir of the yeast and facilitate the dissemination of human C. glabrata strains remains an open question. In this study, MLVA genotyping highlighted the lack of genetic structure of 190 C. glabrata strains isolated from either patients in three hospitals or fecal samples collected from gull breeding colonies located in five distinct areas along the French Mediterranean littoral. Fluconazole-resistant isolates were evenly distributed between both gull and human populations. These findings demonstrate that gulls are a reservoir of this species and facilitate the diffusion of C. glabrata and indirect transmission to human or animal hosts via environmental contamination. This eco-epidemiological view, which can be applied to other vertebrate host species, broadens our perspective regarding the reservoirs and dissemination patterns of antifungal-resistant human pathogenic yeast.

Antimicrobial Resistance of Salmonella Serovars and Campylobacter spp. Isolated from an Opportunistic Gull Species, Yellow-legged Gull ( Larus michahellis ).

Wildlife is a natural reservoir of Salmonella and Campylobacter, the most important human foodborne pathogens worldwide. Free-living birds have the potential to transport, over large distances, such zoonotic bacteria that may harbor antimicrobial resistance traits. On the northeastern Iberian coast, we assessed the role of Yellow-legged Gulls ( Larus michahellis ) as reservoirs of antimicrobial resistance in Salmonella and thermophilic Campylobacter isolates recovered from gulls at three colonies, with varying degrees of dependence on refuse dumps as food sources. Of the 39 Salmonella isolates we tested, 17 were multiresistant (resistance to three antimicrobial families), with eight being Salmonella enterica serovar Typhimurium. Other clinically relevant Salmonella serovars showing multiresistance included Hadar, Bredeney, and Virchow. Relevant Campylobacter antimicrobial resistances were detected among three Campylobacter jejuni isolates, of which all three showed resistance to nalidixic acid, two were resistant to ciprofloxacin, one was resistant to enrofloxacin, and one was resistant to tetracycline. Our results highlight the importance of free-living gulls with opportunistic feeding habits in the dissemination of enteric pathogens resistant to multiple antimicrobial agents of public health concern.

Gut yeast communities in Larus michahellis from various breeding colonies.

Yellow-legged gulls have been reported to carry antibiotic-resistant Enterobacteriaceae; however, the gut mycobiota of these birds has not yet been described. In this study, we analyzed the gut yeast communities in five yellow-legged gull breeding colonies along the Mediterranean littoral in southern France. Gull fecal samples were inoculated onto four types of culture media, including one supplemented with itraconazole. Yeast species richness, abundance, and diversity were estimated, and factorial analysis was used to highlight correspondences between breeding colonies. Yeast grew in 113 of 177 cultures, and 17 distinct yeast species were identified. The most frequent species were Candida krusei (53.5%), Galactomyces geotrichum (44.1%), C. glabrata (40.9%), C. albicans (20.5%), and Saccharomyces cerevisiae (18.1%). Gut yeast community structure in the gulls at both Pierre-Blanche Lagoon (PB) and Frioul Archipelago (F) were characterized by greater species richness and diversity than in those at the two cities of La Grande-Motte (GM) and Palavas-les-Flots (PF) as well as Riou Archipelago (R). Gulls in these latter three sites probably share a similar type of anthropogenic diet. Notably, the proportion of anthropic yeast species, including C. albicans and C. glabrata, in the gull mycobiota increased with gull colony synanthropy. Antifungal resistance was found in each of the five most frequent yeast species. We found that the gut yeast communities of these yellow-legged gulls include antifungal-resistant human pathogens. Further studies should assess the public health impact of these common synanthropic seabirds, which represent a reservoir and disseminator of drug-resistant human pathogenic yeast into the environment.

Liver and muscle esterases as biomarkers of exposure to organophosphate pesticides on yellow-legged gull Larus michahellis (Naumann, 1840) from the Northwest coast of Spain

Liver and muscle esterases as biomarkers of exposure to organophosphate pesticides on yellow-legged gull Larus michahellis (Naumann, 1840) from the Northwest coast of Spain

Assessing the impact of colour-ring codes on parameter estimates from Cormack–Jolly–Seber models: a test with the Yellow-legged Gull (Larus michahellis)

The type of ring (i.e. its colour combination: the colour of the alphanumeric characters and the base colour of the ring) used in population dynamics studies could have an effect on parameters such as resighting probability (p); for instance, we might expect a lower p value when using rings with white characters than when using rings with dark characters. We performed an experiment using two types of colour rings (white or black characters on a dark base) in Yellow-legged Gulls in order to test our hypothesis. To do this, we used Cormack–Jolly–Seber (CJS) models incorporating variation in p among the birds. We obtained no evidence supporting an effect of type of ring on either survival or p.

Long-term trends (1989-2013) in the seabird community breeding in the lagoon of Venice (Italy)

The community of seabirds breeding in the lagoon of Venice, one of the largest around the Mediterranean, was monitored over the 1989-2013 period. Six species have been recorded (<em>Larus michahellis, Chroicocephalus ridibundus, Larus melanocephalus, Sternula albifrons, Sterna hirundo, Sterna sandvicensis</em>). Over the study period, 346 colonies were surveyed; they were located on saltmarsh islets, dredge islands and other artificial sites, in descending order of importance. Beaches were used only at the beginning of the survey. About 4,900 pairs bred in the 2009-2013 years. The community has been always dominated by <em>L</em>. <em>michahellis</em>; in the 2009-2013, this species and <em>S. sandvicensis</em> comprised about 70% of the total. The longterm trends show moderate increase in the size of the whole community. Contrasting trends were observed in different species, with <em>L. michahellis</em>,<em> S. albifrons</em> and <em>S. sandvicensis</em> stable or increasing, whereas <em>C. ridibundus</em> and <em>S. hirundo</em> were declining. The number of pairs nesting on artificial sites increased over the last 15 years, while those on saltmarsh islets decreased correspondingly. This was possibly a response to the increase of mean sea level and storminess observed in the last twenty-five years. <em>S. albifrons</em> and <em>S. sandvicensis</em> populations reached national importance; the population of the latter species is noteworthy at a Mediterranean level.

Feathered Detectives: Real-Time GPS Tracking of Scavenging Gulls Pinpoints Illegal Waste Dumping.

Urban waste impacts human and environmental health, and waste management has become one of the major challenges of humanity. Concurrently with new directives due to manage this human by-product, illegal dumping has become one of the most lucrative activities of organized crime. Beyond economic fraud, illegal waste disposal strongly enhances uncontrolled dissemination of human pathogens, pollutants and invasive species. Here, we demonstrate the potential of novel real-time GPS tracking of scavenging species to detect environmental crime. Specifically, we were able to detect illegal activities at an officially closed dump, which was visited recurrently by 5 of 19 GPS-tracked yellow-legged gulls (Larus michahellis). In comparison with conventional land-based surveys, GPS tracking allows a much wider and cost-efficient spatiotemporal coverage, even of the most hazardous sites, while GPS data accessibility through the internet enables rapid intervention. Our results suggest that multi-species guilds of feathered detectives equipped with GPS and cameras could help fight illegal dumping at continental scales. We encourage further experimental studies, to infer waste detection thresholds in gulls and other scavenging species exploiting human waste dumps.

Trophic strategies of Yellow-legged Gull Larus michahellis on oceanic islands surrounded by deep waters

ABSTRACTCapsule: The diet of Yellow-legged Gulls Larus michahellis on an oceanic island, surrounded by deep waters without a wide shelf, was mainly composed of terrestrial invertebrates.Aims: To study the trophic ecology of Yellow-legged Gulls on an island surrounded by deep waters, to quantify the importance of terrestrial prey items and their availability, and to evaluate the relative importance of nutritional values of terrestrial and marine resources.Methods: Diet was monitored for one year. We assessed the relative contribution of the main prey items and their macronutrients through the study of pellets and faeces.Results: Terrestrial invertebrates were the most frequently consumed prey items (frequency of occurrence (FO) 67%), followed by marine fish (Osteichthyes FO 33%). Coleoptera and Orthoptera were the most consumed terrestrial invertebrates and provided a high nutritional value. The rate of consumption of terrestrial invertebrates varied in synchrony with the breeding season, being higher in spring, indicating their potential importance for reproduction.Conclusion: It is unusual that terrestrial invertebrates constitute a large proportion of the diet of large gulls, but they seemed to cover their trophic energy requirements during the reproductive period.

Assortative mating for carotenoid colouration but not size in the Yellow-legged Gull Larus michahellis

ABSTRACTCapsule: Mediterranean Yellow-legged Gulls mate assortatively according to carotenoid-based colouration but not in relation to size.

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

ABSTRACTCapsule: Chick growth rates was sex-dependent in an Atlantic Yellow-legged Gull Larus michahellis population.Aims: To describe the growth rate of Yellow-legged Gull chicks and sex-associated variations, and obtain a discriminant function to sex them using morphological data.Methods: Fifty-two Yellow-legged Gull chicks from a colony in northern Iberia were measured for body mass, head and bill length, tarsus length and three other bill-length associated variables, from the hatching date up to the age of 36 days. Birds were sexed using DNA analysis.Results: Using logistic models, chick growth rates was observed to be similar between the sexes, while the asymptote was higher among males for the majority of the variables. Discriminant analyses showed that the variable head+bill was very reliable to predict the sex of >80% of chicks at an early developmental stage, and 100% of chicks if combined with tarsus length and two more bill-length associated variables at the age of 35 days.Conclusions: This is the first study using a discriminant analysis to sex Yellow-legged Gull chicks, and also the first to describe the growth function for the species. The growth rate varied between sexes because males showed higher asymptote values within the growth function.

Toxoplasma gondii Infection in Seagull Chicks Is Related to the Consumption of Freshwater Food Resources.

Understanding the spread of Toxoplasma gondii (T. gondii) in wild birds, particularly in those with opportunistic feeding behavior, is of interest for elucidating the epidemiological involvement of these birds in the maintenance and dissemination of the parasite. Overall, from 2009 to 2011, we collected sera from 525 seagull chicks (Yellow-legged gull (Larus michahellis) and Audouin’s gull (L. audouinii)) from 6 breeding colonies in Spain and tested them using the modified agglutination test (MAT) for the presence of antibodies against T. gondii. Chick age was estimated from bill length. Main food source of seagull chicks was evaluated using stable isotope analyses from growing scapular feathers. Overall T. gondii seroprevalence was 21.0% (IC95% 17.5–24.4). A generalized linear mixed-effects model indicated that year (2009) and food source (freshwater) were risk factors associated to the individual risk of infection by T. gondii, while age (days) was close to significance. Freshwater food origin was related to the highest seroprevalence levels, followed by marine origin, supporting freshwater and sewages as important routes of dispersion of T. gondii. Year differences could indicate fluctuating rates of exposure of seagull chicks to T. gondii. Age ranged from 4 to 30 days and seropositivity tended to increase with age (P = 0.07), supporting that seropositivity is related to T. gondii infection rather than to maternal transfer of antibodies, which in gulls is known to sharply decrease with chick age. This study is the first to report T. gondii antibodies in Yellow-legged and Audouin’s gulls, thereby extending the range of intermediate hosts for this parasite and underscoring the complexity of its epidemiology.

Metal pollution in biotic and abiotic samples of the Büyük Menderes River, Turkey.

The Büyük Menderes River (BMR) is one of the largest rivers in Turkey. This river irrigates efficient farmlands and includes tributaries of other rivers and streams and many populated towns within its limits in the Ege region. Both the estuary and Işıklı Lake serve as a sanctuary for various waterbirds. Therefore, the BMR plays a critical role both for the inhabitants and for the ecosystem organisms in its environs. In the present study, we analyzed levels of metals including iron, barium, zinc, vanadium, cobalt, chromium, cadmium, copper, nickel, aluminum, arsenic, manganese, antimony, silver, selenium, boron, mercury, titanium, and lead in river water, sediment, fish (Cyprinus carpio; common carp), and in various waterbird (Fulica atra, Euroasian coot; Larus michahellis, yellow-legged gull; Ardea cinerea, grey heron; Larus melanocephalus, Mediterranean gull; and Pelecanus crispus, pelican) samples. Analyses were performed using an inductively coupled plasma-mass spectrometry (ICP-MS) instrument after sample preparation. Comparing metal concentrations among different sample types, it was found that barium, aluminum, and zinc are the major metals in river water, and zinc in common carp muscle, while iron, aluminum, and manganese are the major metals in sediments. Iron, zinc, copper, and aluminum were the highest in waterbird muscle tissue. Iron and barium were found to be the major metals in eggshell, while iron and zinc are the major metals in egg samples. A simple "worst-case scenario" model of risk assessment revealed that some of the analyzed metals may pose a risk for human health through consuming fish.

The eagle owl Bubo bubo (Aves: Strigidae) in the Eastern Adriatic (Croatia): the study case of a high-density insular population

The Croatian population of the eagle owl Bubo bubo (Linnaeus, 1758) is estimated at 800–1200 breeding pairs with the majority of population breeding in the Mediterranean region, along the eastern Adriatic coast. The main aims of this work were two-fold: (1) to determine the eagle owl territorial densities in the central part of Mediterranean Croatia; and (2) to examine landscape composition and configuration of the study plots and consider possible reasons for differences in recorded densities. The abundance of the eagle owl was surveyed from 2001 to 2006 within three plots of similar size (a total survey area of 246 km2): two plots were on the mainland and one on the archipelago at about 16 km from the coast. The playback method was used to stimulate eagle owl territorial behaviour and to determine the locations of their territories. Territorial densities ranged from 4.5 to 26.2 pairs/100 km2, with the highest density being recorded on islands. We suggest that this high density is a result of good foraging conditions, especially year-round availability and high abundance of the yellow-legged gull Larus michahellis J. F. Naumann, 1840 and the brown rat Rattus rattus (Linnaeus, 1758), together with low risk of human-induced mortality.