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.

Trophic versus geographic structure in stable isotope signatures of pelagic seabirds breeding in the northeast Atlantic

Feeding ecology and geographic location are 2 major factors influencing animal stable isotope signatures, but their relative contributions are poorly understood, which limits the usefulness of stable isotope analysis in the study of animal ecology. To improve our knowledge of the main sources of isotopic variability at sea, we determined δ15N and δ13C signatures in the first primary feather of adult birds from 11 Procellariiform species (n = 609) across 16 northeast Atlantic localities, from Cape Verde (20°N) to Iceland (60°N). Post-breeding areas (where the studied feather is thought to be grown) were determined using light-level geolocation for 6 of the 11 species. Isotopic variability was geographically unstructured within the mid-northeast Atlantic (Macaronesian archipelagos), but trophically structured according to species and regardless of the breeding location, presumably as a result of trophic segregation among species. Indeed, the interspecific isotopic overlap resulting from combining δ15N and δ13C signatures of seabirds was low, which suggests that most species exploited exclusive trophic resources consistently across their geographic range. Species breeding in north temperate regions (Iceland, Scotland and Northern Ireland) showed enriched δ15N compared to the same or similar species breeding in tropical and subtropical regions, suggesting some differences in baseline levels between these regions. The present study illustrates a noticeable trophic segregation of northeast Atlantic Procellariiformes. Our results show that the isotopic approach has limited applicability for the study of animal movements in the northeast Atlantic at a regional scale, but is potentially useful for the study of long-distance migrations between large marine systems

Effects of extra mass on the pelagic behavior of a seabird

Satellite transmitters and geographic-positioning-system devices often add substantial mass to birds to which they are attached. Studies on the effects of such instruments have focused on indirect measures, whereas the direct influence of extra mass on pelagic behavior is poorly known. We used 2.5-g geolocators to investigate the effect of extra mass on the pelagic behavior of Cory's Shearwaters (Calonectris diomedea) by comparing the traits of a single foraging trip among a group carrying 30-g weights, a group carrying 60-g weights, and a control group. The weights were attached to the birds' backs using typical techniques for attaching satellite transmitters to seabirds. The extra mass increased the duration of the birds' trips and decreased their foraging efficiency and mass gained at sea. These indirect effects may be related to foraging traits: weighted birds showed a greater search effort than control birds, traveled greater distances, covered a greater foraging area, and increased the maximum foraging range. Furthermore, the time spent on the sea surface at night was greater for weighted than for control groups, which showed that the extra mass also affected activity patterns. Our results underline the need to quantify the effects of monitoring equipment commonly used to study the pelagic behavior of seabirds. We suggest that geolocators can be used to obtain control data on foraging-trip movements and activity patterns.

Nutritional and feeding ecology in the Cory"s shearwater (Calonectris diomedea).

In birds, parents adjust their feeding behaviour according to breeding duties, which ultimately may lead to seasonal adjustments in nutritional physiology and hematology over the breeding season. Although avian physiology has been widely investigated in captivity, few studies have integrated individual changes in feeding and physiological ecology throughout the breeding season in wild birds. To study relationships between feeding ecology and nutritional ecophysiology in Cory"s shearwater Calonectris diomedea, we weighed and took blood samples from 28 males and 19 females during the pre-laying, egg-laying, incubation, hatching and chick-rearing periods of the breeding season. In addition, we fitted 6 birds with geolocators to track their foraging movements throughout the reproductive period. Thus, we examined individual changes in (1) nutritional condition (biochemistry metabolites); (2) oxygen carrying capacity (hematology); and (3) feeding areas and foraging effort (stable isotopes and foraging movements). Geolocators revealed a latitudinal shift in main feeding areas towards more southern and more neritic waters throughout the breeding season, which is consistent with the steady increase in δ13C signatures in the blood. Geolocators also showed a decrease in foraging effort from egg-laying to hatching, reflecting the activity decrease associated with incubation duties. Plasma metabolites, body mass and oxygen carrying capacity were associated with temporal changes in nutritional state and foraging effort in relation to recovery after migration, egg formation, fasting shifts during incubation and chick provisioning. This study shows that combining physiological and ecological approaches can help us understand the influence of breeding duties on feeding ecology and nutritional physiology in wild birds.

Geographic assignment of seabirds to their origin: combining morphology, genetics and biogeochemical analyses

Longline fisheries, oil spills, and offshore wind farms are some of the major threats increasing seabird mortality at sea, but the impact of these threats on specific populations has been difficult to determine so far. We tested the use of molecular markers, morphometric measures, and stable isotope (δ15N and δ13C) and trace element concentrations in the first primary feather (grown at the end of the breeding period) to assign the geographic origin of Calonectris shearwaters. Overall, we sampled birds from three taxa: 13 Mediterranean Cory's Shearwater (Calonectris diomedea diomedea) breeding sites, 10 Atlantic Cory's Shearwater (Calonectris diomedea borealis) breeding sites, and one Cape Verde Shearwater (C. edwardsii) breeding site. Assignment rates were investigated at three spatial scales: breeding colony, breeding archipelago, and taxa levels. Genetic analyses based on the mitochondrial control region (198 birds from 21 breeding colonies) correctly assigned 100% of birds to the three main taxa but failed in detecting geographic structuring at lower scales. Discriminant analyses based on trace elements composition achieved the best rate of correct assignment to colony (77.5%). Body measurements or stable isotopes mainly succeeded in assigning individuals among taxa (87.9% and 89.9%, respectively) but failed at the colony level (27.1% and 38.0%, respectively). Combining all three approaches (morphometrics, isotopes, and trace elements on 186 birds from 15 breeding colonies) substantially improved correct classifications (86.0%, 90.7%, and 100% among colonies, archipelagos, and taxa, respectively). Validations using two independent data sets and jackknife cross-validation confirmed the robustness of the combined approach in the colony assignment (62.5%, 58.8%, and 69.8% for each validation test, respectively). A preliminary application of the discriminant model based on stable isotope δ15N and δ13C values and trace elements (219 birds from 17 breeding sites) showed that 41 Cory's Shearwaters caught by western Mediterranean long-liners came mainly from breeding colonies in Menorca (48.8%), Ibiza (14.6%), and Crete (31.7%). Our findings show that combining analyses of trace elements and stable isotopes on feathers can achieve high rates of correct geographic assignment of birds in the marine environment, opening new prospects for the study of seabird mortality at sea.

Trans-equatorial migration and mixing in the wintering areas of a pelagic seabird

Despite increasing interest in long-distance migration, the wintering areas, migration corridors, and population mix in winter quarters of most pelagic marine predators are unknown. Here, we present the first study tracking migration movements of shearwaters through the non-breeding period. We used geolocators (global location sensing [GLS] units based on ambient light levels) to track 22 Cory's shearwaters (Calonectris diomedea) breeding in three different areas. Most birds wintered in one or more of three relatively small areas, all clearly associated with major coastal upwelling systems of the tropical and south Atlantic. Trans-equatorial movements were dominated by prevailing trade winds and westerlies, while calm, oligotrophic areas were avoided. Breeding populations clearly differed in their preference amongst the three major wintering areas, but showed substantial mixing. This illustrates the exceptional value of GLS, not only for determining and describing the influence of oceanographic features on migration patterns, but also for assessing population mix in winter quarters. This knowledge is essential to understanding the impacts of population-level threats, such as longlining, offshore windfarms, and oil spills on multiple breeding sites, and will be critical in devising conservation policies that guarantee the sustainable exploitation of the oceans.

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.

Ecological and physiological variance in T-cell mediated immune response in Cory's shearwaters

T-cell mediated immune response (CMI) hasbeen widely studied in relation to individual andfitness components in birds. However, few studieshave simultaneously examined individual and socialfactors and habitat-mediated variance in theimmunity of chicks and adults from the samepopulation and in the same breeding season. Weinvestigated ecological and physiological variancein CMI of male and female nestlings and adults in abreeding population of Cory's Shearwaters(Calonectrisdiomedea) in theMediterranean Sea. Explanatory variables includedindividual traits (body condition, carbon andnitrogen stable isotope ratios, plasma totalproteins, triglycerides, uric acid, osmolarity,β-hydroxy-butyrate, erythrocyte meancorpuscular diameter, hematocrit, andhemoglobin) and burrow traits(temperature, isolation, and physicalstructure). During incubation, immune responseof adult males was significantly greater than thatof females. Nestlings exhibited a lower immuneresponse than adults. Ecological and physiologicalfactors affecting immune response differed betweenadults and nestlings. General linear models showedthat immune response in adult males was positivelyassociated with burrow isolation, suggesting thatmales breeding at higher densities suffer immunesystem suppression. In contrast, immune response inchicks was positively associated with bodycondition and plasma triglyceride levels.Therefore, adult immune response appears to beassociated with social stress, whereas a trade-offbetween immune function and fasting capability mayexist for nestlings. Our results, and those fromprevious studies, provide support for anasymmetrical influence of ecological andphysiological factors on the health of differentage and sex groups within a population, and for theimportance of simultaneously considering individualand population characteristics in intraspecificstudies of immune response.

Parental body condition does not correlate with offspring sex-ratio in Cory's shearwater

We analyzed offspring sex ratio variation in Mediterranean Cory's Shearwater (Calonectris d. diomedea) during two consecutive breeding seasons in two colonies. We test for differential breeding conditions between years and colonies looking at several breeding parameters and parental condition. We then explored the relationship between offspring sex ratio and parental condition and breeding parameters. This species is sexually dimorphic with males larger and heavier than females; consequently we expected differential parental cost in rearing sexes, or a greater sensitivity of male chicks to adverse conditions, which may lead to biased sex ratios. Chicks were sexed molecularly by the amplification of the CHD genes. Offspring sex ratio did not differ from parity, either at hatching or fledging, regardless of the colony or year. However, parental body condition and breeding parameters such as egg size and breeding success were different between years and colonies. Nevertheless, neither nestling mortality nor body condition at fledging varied between years or colonies, suggesting that male and female chicks were probably not differentially affected by variability in breeding conditions.

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.

Ecological and physiological variance in T-cell mediated immune response in Cory's shearwaters

T-cell mediated immune response (CMI) hasbeen widely studied in relation to individual andfitness components in birds. However, few studieshave simultaneously examined individual and socialfactors and habitat-mediated variance in theimmunity of chicks and adults from the samepopulation and in the same breeding season. Weinvestigated ecological and physiological variancein CMI of male and female nestlings and adults in abreeding population of Cory's Shearwaters(Calonectrisdiomedea) in theMediterranean Sea. Explanatory variables includedindividual traits (body condition, carbon andnitrogen stable isotope ratios, plasma totalproteins, triglycerides, uric acid, osmolarity,β-hydroxy-butyrate, erythrocyte meancorpuscular diameter, hematocrit, andhemoglobin) and burrow traits(temperature, isolation, and physicalstructure). During incubation, immune responseof adult males was significantly greater than thatof females. Nestlings exhibited a lower immuneresponse than adults. Ecological and physiologicalfactors affecting immune response differed betweenadults and nestlings. General linear models showedthat immune response in adult males was positivelyassociated with burrow isolation, suggesting thatmales breeding at higher densities suffer immunesystem suppression. In contrast, immune response inchicks was positively associated with bodycondition and plasma triglyceride levels.Therefore, adult immune response appears to beassociated with social stress, whereas a trade-offbetween immune function and fasting capability mayexist for nestlings. Our results, and those fromprevious studies, provide support for anasymmetrical influence of ecological andphysiological factors on the health of differentage and sex groups within a population, and for theimportance of simultaneously considering individualand population characteristics in intraspecificstudies of immune response.

Research Priorities for seabirds: Improving seabird conservation and management in the 21st century

Seabirds are facing a growing number of threats in both terrestrial and marine habitats, and many populations have experienced dramatic changes over past decades. Years of seabird research have improved our understanding of seabird populations and provided a broader understanding of marine ecological processes. In an effort to encourage future research and guide seabird conservation science, seabird researchers from 9 nations identified the 20 highest priority research questions and organized these into 6 general categories: (1) population dynamics, (2) spatial ecology, (3) tropho-dynamics, (4) fisheries interactions, (5) response to global change, and (6) management of anthropogenic impacts (focusing on invasive species, contaminants and protected areas). For each category, we provide an assessment of the current approaches, challenges and future directions. While this is not an exhaustive list of all research needed to address the myriad conservation challenges seabirds face, the results of this effort represent an important synthesis of current expert opinion across sub-disciplines within seabird ecology. As this synthesis highlights, research, in conjunction with direct management, education, and community engagement, can play an important role in facilitating the conservation and management of seabird populations and of the ocean ecosystems on which they and we depend.

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.

Population structure in a highly pelagic seabird, the Cory's shearwater (Calonectris diomedea): an examination of genetics, morphology and ecology

Increasing evidence suggests oceanic traits may play a key role in the genetic structuring of marine organisms. Whereas genetic breaks in the open ocean are well known in fishes and marine invertebrates, the importance of marine habitat characteristics in seabirds remains less certain. We investigated the role of oceanic transitions versus population genetic processes in driving population differentiation in a highly vagile seabird, the Cory"s shearwater, combining molecular, morphological and ecological data from 27 breeding colonies distributed across the Mediterranean (Calonectris diomedea diomedea) and the Atlantic (C. d. borealis). Genetic and biometric analyses showed a clear differentiation between Atlantic and Mediterranean Cory"s shearwaters. Ringing-recovery data indicated high site fidelity of the species, but we found some cases of dispersal among neighbouring breeding sites (<300 km) and a few long distance movements (>1000 km) within and between each basin. In agreement with this, comparison of phenotypic and genetic data revealed both current and historical dispersal events. Within each region, we did not detect any genetic substructure among archipelagos in the Atlantic, but we found a slight genetic differentiation between western and eastern breeding colonies in the Mediterranean. Accordingly, gene flow estimates suggested substantial dispersal among colonies within basins. Overall, genetic structure of the Cory"s shearwater matches main oceanographic breaks (Almería-Oran Oceanic Front and Siculo-Tunisian Strait), but spatial analyses suggest that patterns of genetic differentiation are better explained by geographic rather than oceanographic distances. In line with previous studies, genetic, phenotypic and ecological evidence supported the separation of Atlantic and Mediterranean forms, suggesting the 2 taxa should be regarded as different species.