Circulation of a Meaban-like virus in yellow-legged gulls and seabird ticks in the western Mediterranean Basin

In recent years, a number of zoonotic flaviviruses have emerged worldwide, and wild birds serve as their major reservoirs. Epidemiological surveys of bird populations at various geographical scales can clarify key aspects of the eco-epidemiology of these viruses. In this study, we aimed at exploring the presence of flaviviruses in the western Mediterranean by sampling breeding populations of the yellow-legged gull (Larus michahellis), a widely distributed, anthropophilic, and abundant seabird species. For 3 years, we sampled eggs from 19 breeding colonies in Spain, France, Algeria, and Tunisia. First, ELISAs were used to determine if the eggs contained antibodies against flaviviruses. Second, neutralization assays were used to identify the specific flaviviruses present. Finally, for colonies in which ELISA-positive eggs had been found, chick serum samples and potential vectors, culicid mosquitoes and soft ticks (Ornithodoros maritimus), were collected and analyzed using serology and PCR, respectively. The prevalence of flavivirus-specific antibodies in eggs was highly spatially heterogeneous. In northeastern Spain, on the Medes Islands and in the nearby village of L'Escala, 56% of eggs had antibodies against the flavivirus envelope protein, but were negative for neutralizing antibodies against three common flaviviruses: West Nile, Usutu, and tick-borne encephalitis viruses. Furthermore, little evidence of past flavivirus exposure was obtained for the other colonies. A subset of the Ornithodoros ticks from Medes screened for flaviviral RNA tested positive for a virus whose NS5 gene was 95% similar to that of Meaban virus, a flavivirus previously isolated from ticks of Larus argentatus in western France. All ELISA-positive samples subsequently tested positive for Meaban virus neutralizing antibodies. This study shows that gulls in the western Mediterranean Basin are exposed to a tick-borne Meaban-like virus, which underscores the need of exploring the spatial and temporal distribution of this flavivirus as well as its potential pathogenicity for animals and humans.

Population connectivity buffers genetic diversity loss in a seabird

Background Ancient DNA has revolutionized conservation genetic studies as it allows monitoring of the genetic variability of species through time and predicting the impact of ecosystems" threats on future population dynamics and viability. Meanwhile, the consequences of anthropogenic activities and climate change to island faunas, particularly seabirds, remain largely unknown. In this study, we examined temporal changes in the genetic diversity of a threatened seabird, the Cory"s shearwater (Calonectris borealis). Findings We analysed the mitochondrial DNA control region of ancient bone samples from the late-Holocene retrieved from the Canary archipelago (NE Atlantic) together with modern DNA sequences representative of the entire breeding range of the species. Our results show high levels of ancient genetic diversity in the Canaries comparable to that of the extant population. The temporal haplotype network further revealed rare but recurrent long-distance dispersal between ocean basins. The Bayesian demographic analyses reveal both regional and local population size expansion events, and this is in spite of the demographic decline experienced by the species over the last millennia. Conclusions Our findings suggest that population connectivity of the species has acted as a buffer of genetic losses and illustrate the use of ancient DNA to uncover such cryptic genetic events.

Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different foodwebs

We investigated trophic ecology variation among colonies as well as sex- and age-related differences in the diet of the southern giant petrel Macronectes giganteus, a long-lived seabird that is sexually dimorphic in size. We measured stable isotopes (δ13C, δ15N) in blood samples collected during breeding at Bird Island (South Georgia, Antarctica) in 1998 and at 2 colonies in the Argentinean area of Patagonia in 2000 and 2001. Individuals from South Georgia showed lower δ13C and δ15N values than those in Patagonia, as expected from the more pelagic location and the short length of the Antarctic food web. Males and females showed significant differences in the isotopic signatures at both localities. These differences agree with the sexual differences in diet found in previous studies, which showed that both sexes rely mainly on penguin and seal carrion, but females also feed extensively on marine prey, such as fish, squid and crustaceans. However, males from Patagonia showed significantly higher δ15N and δ13C values than females did, and the reverse trend was observed at South Georgia. This opposite trend is probably related to the different trophic level of carrion between locations: whereas penguins and pinnipeds in Patagonia rely mainly on fish and cephalopods, in South Georgia they rely mainly on krill. Stable isotope values of male and female chicks in Patagonia did not differ; both attained high values, similar to adult males and higher than adult females, suggesting that parents do not provision their single offspring differently in relation to sex; however, they seem to provide offspring with a higher proportion of carrion, probably of higher quality, and more abundant food, than they consume themselves. Stable isotopes at South Georgia were not affected by age of adults. We have provided new information on intraspecific segregation in the diet in a seabird species and have also underlined the importance of considering food web structure when studying intraspecific variability in trophic ecology.

Metals and Selenium as bioindicators of geographic and trophic segregation in Giant Petrels Macronectes spp.

We analysed concentrations of cadmium, lead, mercury and selenium in blood from males and females of the 2 sibling species of giant petrels, the northern Macronectes halli and the southern M. giganteus, breeding sympatrically at Bird Island (South Georgia, Antarctica). Blood samples were collected in 1998 during the incubation period, from 5 November to 10 December. Between species, cadmium and lead concentrations were significantly higher for northern than for southern giant petrels, which probably resulted from northern giant petrels wintering in more polluted areas (mainly on the Patagonian Shelf and Falkland Islands) compared to southern giant petrels (wintering mainly around South Georgia and the South Sandwich Islands). Between sexes, cadmium concentrations were significantly higher for females than for males in both species, corresponding to the more pelagic habits of females compared to the more scavenging habits of males. Lead and cadmium concentrations in circulating blood decreased significantly over the incubation period, suggesting that when breeding at Bird Island, exposure to the source of pollution had ended, and these metals had been cleared from the blood and excreted, or rapidly transferred to other tissues. Association of lead and cadmium with a common source of pollution was further corroborated by a significant positive correlation between the levels of the 2 elements found. Mercury levels were similar between the species, but showed an opposite trend between sexes, with males showing higher levels than females in northern giant petrels, and the opposite was true in southern giant petrels, with no changes throughout incubation. Selenium levels were similar between sexes, but significantly greater for northern than for southern giant petrels. Moreover, there was a significant increase in the selenium levels over the incubation period in northern giant petrels. Age of adult birds did not affect metal concentrations. Coefficients of variation of metal levels were consistently lower for northern than for southern giant petrels, particularly for mercury, suggesting that the former species is more dietary specialised than the latter. Contaminant analyses, when combined with accurate information on seabird movements, obtained through geolocation or satellite tracking, help us to understand geographic variation of pollution in the marine environment.

Feather mercury levels in seabirds at South Georgia: Influences of trophic position, sex and age

We studied the mercury contamination of 13 species of seabirds breeding on Bird Island, South Georgia, in 1998. Total mercury concentrations in body feather samples of birds caught at their breeding colonies were determined. Among the species, grey-headed albatross (8933 ng g-1) and southern giant petrel (7774 ng g-1) showed the highest, and gentoo penguin (948 ng g-1) the lowest body feather mercury concentrations. Mercury levels were negatively correlated with the proportion of crustaceans (mainly krill) in the species¹ diets, suggesting that the trophic level is the most important factor in explaining the variation of mercury concentrations in Antarctic seabirds. In 4 species studied for age effects among adult birds (grey-headed and black-browed albatross, northern and southern giant petrel), no age-dependent variation in mercury levels was found. Sex differences were also assessed: female gentoo penguins had lower mercury levels than males, which may be related to the elimination of part of the mercury body burden by females into eggs. In contrast, northern giant petrel males had lower levels than females, which may be related to a higher consumption by males of carrion from Antarctic fur seals. In grey-headed albatrosses, mercury levels were 113% higher than in 1989, when this species was investigated at the same site, indicating a possible increase in mercury pollution of the Southern Ocean during the last decade.

Influence of sea surface winds on shearwater migration detours

To test the potential effects of winds on the migratory detours of shearwaters, transequatorial migrations of 3 shearwaters, the Manx Puffinus puffinus, the Cory"s Calonectris diomedea, and the Cape Verde C. edwardsii shearwaters were tracked using geolocators. Concurrent data on the direction and strength of winds were obtained from the NASA SeaWinds scatterometer to calculate daily impedance models reflecting the resistance of sea surface winds to the shearwater movements. From these models we estimated relative wind-mediated costs for the observed synthesis pathway obtained from tracked birds, for the shortest distance pathway and for other simulated alternative pathways for every day of the migration period. We also estimated daily trajectories of the minimum cost pathway and compared distance and relative costs of all pathways. Shearwaters followed 26 to 52% longer pathways than the shortest distance path. In general, estimated wind-mediated costs of both observed synthesis and simulated alternative pathways were strongly dependent on the date of departure. Costs of observed synthesis pathways were about 15% greater than the synthesis pathway with the minimum cost, but, in the Cory"s and the Cape Verde shearwaters, these pathways were on average 15 to 20% shorter in distance, suggesting the extra costs of the observed pathways are compensated by saving about 2 travelling days. In Manx shearwaters, however, the distance of the observed synthesis pathway was 25% longer than that of the lowest cost synthesis pathway, probably because birds avoided shorter but potentially more turbulent pathways. Our results suggest that winds are a major determinant of the migratory routes of seabirds.

Ten years after the Prestige Oil Spill: seabird trophic ecology as indicator of long-term effects on the coastal marine ecosystem

Major oil spills can have long-term impacts since oil pollution does not only result in acute mortality of marine organisms, but also affects productivity levels, predator-prey dynamics, and damages habitats that support marine communities. However, despite the conservation implications of oil accidents, the monitoring and assessment of its lasting impacts still remains a difficult and daunting task. Here, we used European shags to evaluate the overall, lasting effects of the Prestige oil spill (2002) on the affected marine ecosystem. Using δ15N and Hg analysis, we trace temporal changes in feeding ecology potentially related to alterations of the food web due to the spill. Using climatic and oceanic data, we also investigate the influence of North Atlantic Oscillation (NAO) index, the sea surface temperature (SST) and the chlorophyll a (Chl a) on the observed changes. Analysis of δ15N and Hg concentrations revealed that after the Prestige oil spill, shag chicks abruptly switched their trophic level from a diet based on a high percentage of demersal-benthic fish to a higher proportion of pelagic/semi-pelagic species. There was no evidence that Chl a, SST and NAO reflected any particular changes or severity in environmental conditions for any year or season that may explain the sudden change observed in trophic level. Thus, this study highlighted an impact on the marine food web for at least three years. Our results provide the best evidence to date of the long-term consequences of the Prestige oil spill. They also show how, regardless of wider oceanographic variability, lasting impacts on predator-prey dynamics can be assessed using biochemical markers. This is particularly useful if larger scale and longer term monitoring of all trophic levels is unfeasible due to limited funding or high ecosystem complexity.

Trophic structure in a seabird host-parasite food web: insights from stable isotope analyses

Ecological studies on food webs rarely include parasites, partly due to the complexity and dimensionality of host-parasite interaction networks. Multiple co-occurring parasites can show different feeding strategies and thus lead to complex and cryptic trophic relationships, which are often difficult to disentangle by traditional methods. We analyzed stable isotope ratios of C (13C/12C, δ13C) and N (15N/14N, δ15N) of host and ectoparasite tissues to investigate trophic structure in 4 co-occurring ectoparasites: three lice and one flea species, on two closely related and spatially segregated seabird hosts (Calonectris shearwaters). δ13C isotopic signatures confirmed feathers as the main food resource for the three lice species and blood for the flea species. All ectoparasite species showed a significant enrichment in δ15N relatively to the host tissue consumed (discrimination factors ranged from 2 to 5 depending on the species). Isotopic differences were consistent across multiple host-ectoparasite locations, despite of some geographic variability in baseline isotopic levels. Our findings illustrate the influence of both ectoparasite and host trophic ecology in the isotopic structuring of the Calonectris ectoparasite community. This study highlights the potential of stable isotope analyses in disentangling the nature and complexity of trophic relationships in symbiotic systems.

Ancient DNA of the extinct Lava shearwater (Puffinus olsoni) from the Canary Islands reveals incipient differentiation within the P. puffinus complex

The loss of species during the Holocene was, dramatically more important on islands than on continents. Seabirds from islands are very vulnerable to human-induced alterations such as habitat destruction, hunting and exotic predators. For example, in the genus Puffinus (family Procellariidae) the extinction of at least five species has been recorded during the Holocene, two of them coming from the Canary Islands.

Ocean surface winds drive dynamics of transoceanic aerial movements

Global wind patterns influence dispersal and migration processes of aerial organisms, propagules and particles, which ultimately could determine the dynamics of colonizations, invasions or spread of pathogens. However, studying how wind-mediated movements actually happen has been hampered so far by the lack of high resolution global wind data as well as the impossibility to track aerial movements. Using concurrent data on winds and actual pathways of a tracked seabird, here we show that oceanic winds define spatiotemporal pathways and barriers for large-scale aerial movements. We obtained wind data from NASA SeaWinds scatterometer to calculate wind cost (impedance) models reflecting the resistance to the aerial movement near the ocean surface. We also tracked the movements of a model organism, the Cory's shearwater (Calonectris diomedea), a pelagic bird known to perform long distance migrations. Cost models revealed that distant areas can be connected through"wind highways" that do not match the shortest great circle routes. Bird routes closely followed the low-cost"wind-highways" linking breeding and wintering areas. In addition, we found that a potential barrier, the near surface westerlies in the Atlantic sector of the Intertropical Convergence Zone (ITCZ), temporally hindered meridional trans-equatorial movements. Once the westerlies vanished, birds crossed the ITCZ to their winter quarters. This study provides a novel approach to investigate wind-mediated movements in oceanic environments and shows that large-scale migration and dispersal processes over the oceans can be largely driven by spatiotemporal wind patterns.

Understanding oceanic migrations with intrinsic biogeochemical markers

Migratory marine vertebrates move annually across remote oceanic water masses crossing international borders. Many anthropogenic threats such as overfishing, bycatch, pollution or global warming put millions of marine migrants at risk especially during their long-distance movements. Therefore, precise knowledge about these migratory movements to understand where and when these animals are more exposed to human impacts is vital for addressing marine conservation issues. Because electronic tracking devices suffer from several constraints, mainly logistical and financial, there is emerging interest in finding appropriate intrinsic markers, such as the chemical composition of inert tissues, to study long-distance migrations and identify wintering sites. Here, using tracked pelagic seabirds and some of their own feathers which were known to be grown at different places and times within the annual cycle, we proved the value of biogeochemical analyses of inert tissue as tracers of marine movements and habitat use. Analyses of feathers grown in summer showed that both stable isotope signatures and element concentrations can signal the origin of breeding birds feeding in distinct water masses. However, only stable isotopes signalled water masses used during winter because elements mainly accumulated during the long breeding period are incorporated into feathers grown in both summer and winter. Our findings shed new light on the simple and effective assignment of marine organisms to distinct oceanic areas, providing new opportunities to study unknown migration patterns of secretive species, including in relation to human-induced mortality on specific populations in the marine environment.

Comparing multiple criteria for species identification in two recently diverged seabirds

Correct species identification is a crucial issue in systematics with key implications for prioritising conservation effort. However, it can be particularly challenging in recently diverged species due to their strong similarity and relatedness. In such cases, species identification requires multiple and integrative approaches. In this study we used multiple criteria, namely plumage colouration, biometric measurements, geometric morphometrics, stable isotopes analysis (SIA) and genetics (mtDNA), to identify the species of 107 bycatch birds from two closely related seabird species, the Balearic (Puffinus mauretanicus) and Yelkouan (P. yelkouan) shearwaters. Biometric measurements, stable isotopes and genetic data produced two stable clusters of bycatch birds matching the two study species, as indicated by reference birds of known origin. Geometric morphometrics was excluded as a species identification criterion since the two clusters were not stable. The combination of plumage colouration, linear biometrics, stable isotope and genetic criteria was crucial to infer the species of 103 of the bycatch specimens. In the present study, particularly SIA emerged as a powerful criterion for species identification, but temporal stability of the isotopic values is critical for this purpose. Indeed, we found some variability in stable isotope values over the years within each species, but species differences explained most of the variance in the isotopic data. Yet this result pinpoints the importance of examining sources of variability in the isotopic data in a case-by-case basis prior to the cross-application of the SIA approach to other species. Our findings illustrate how the integration of several methodological approaches can help to correctly identify individuals from recently diverged species, as each criterion measures different biological phenomena and species divergence is not expressed simultaneously in all biological traits.

Feeding ecology and movements of the Barolo shearwater Puffinus baroli baroli in the Azores, NE Atlantic

Trophic ecology and movements are critical issues for understanding the role of marine predators in food webs and for facing the challenges of their conservation. Seabird foraging ecology has been increasingly studied, but small elusive species, such as those forming the"little shearwater" complex, remain poorly known. We present the first study on the movements and feeding ecology of the Barolo shearwater Puffinus baroli baroli in a colony from the Azores archipelago (NE Atlantic), combining global location-sensing units, stable isotope analyses of feathers (δ13C and δ15N), stomach flushings and data from maximum depth gauges. During the chick-rearing period, parents visited their nests most nights, foraged mainly south of the colony and fed at lower trophic levels than during the non-breeding period. Squid was the most diverse prey (6 families and at least 10 different taxa), but species composition varied considerably between years. Two squid families, Onychoteuthidae and Argonautidae, and the fish family Phycidae accounted for 82.3% of ingested prey by number. On average, maximum dive depths per foraging trip reached 14.8 m (range: 7.9 to 23.1 m). After the breeding period, birds dispersed offshore in all directions and up to 2500 km from the breeding colony, and fed at higher trophic levels. Overall, our results indicate that the Barolo shearwater is a non-migratory shearwater feeding at the lowest trophic level among Macaronesian seabirds, showing both diurnal and nocturnal activity and feeding deeper in the water column, principally on small schooling squid and fish. These traits contrast with those of 3 other Azorean Procellariiformes (Cory"s shearwater Calonectris diomedea, the Madeiran storm-petrel Oceanodroma castro and Monteiro"s storm-petrel O. monteiroi), indicating ecological segregation within the Azorean seabird community.

Seabirds and the circulation of Lyme borreliosis bacteria in the North Pacific

Seabirds act as natural reservoirs to Lyme borreliosis spirochetes and may play a significant role in the global circulation of these pathogens. While Borrelia burgdorferi sensu lato (Bbsl) has been shown to occur in ticks collected from certain locations in the North Pacific, little is known about interspecific differences in exposure within the seabird communities of this region. We examined the prevalence of anti-Bbsl antibodies in 805 individuals of nine seabird species breeding across the North Pacific. Seroprevalence varied strongly among species and locations. Murres (Uria spp.) showed the highest antibody prevalence and may play a major role in facilitating Bbsl circulation at a worldwide scale. Other species showed little or no signs of exposure, despite being present in multispecific colonies with seropositive birds. Complex dynamics may be operating in this wide scale, natural hostparasite system, possibly mediated by the host immune system and host specialization of the tick vector.

Combining stable isotope analyses and geolocation to reveal kittiwake migration

Determining migratory strategies of seabirds is still a major challenge due to their relative inaccessibility. Small geolocators are improving this knowledge, but not all birds can be tracked. Stable isotope ratios in feathers can help us to understand migration, but we still have insufficient baseline knowledge for linking feather signatures to movements amongst distinct water masses. To understand the migration strategies of kittiwakes Rissa tridactyla and the link between stable isotopes in feathers and the areas in which these were grown, we tracked 6 kittiwakes from Hornøya, Norway, with light level geolocators over 1 yr. Then we analysed the stable isotopes of carbon and nitrogen in their 1st and 7th primary feathers as well as in the 1st, 3rd, 5th, 7th and 10th primaries of 12 birds found freshly dead in the same breeding colony. After breeding, all tracked birds moved east of the Svalbard Archipelago and subsequently migrated to the Labrador Sea. Thereafter, birds showed individual variation in migration strategies: 3 travelled to the NE Atlantic, whereas the others remained in the Labrador Sea until the end of the wintering period. Changes in stable isotope signatures from the 1st to the 10th primary feathers corresponded well to the sequence of movements during migration and the area in which we inferred that each feather was grown. Thus, by combining information on moult patterns and tracking data, we demonstrate that stable isotope analysis of feathers can be used to trace migratory movements of seabirds.