Exposure of an endangered seabird species to persistent organic pollutants: Assessing levels in blood and link with reproductive parameters.

Ocean contamination, particularly from persistent organic pollutants (POPs), remains a significant threat to marine predators that occupy high trophic positions. Long-lived procellariform seabirds are apex predators in marine ecosystems and tend to accumulate contaminants. Prolonged exposure to pollutants negatively affects their fitness including reproductive success. Low breeding success may represent a hurdle for the restoration of small and endangered seabird populations, including several highly threatened gadfly petrels. Here we investigated the annual variation (2019 and 2022) in organochlorine pesticide (OCP), polychlorinated biphenyl ether (PCB), polybrominated diphenyl ether (PBDE), and polycyclic aromatic hydrocarbon (PAH) exposure in the endangered Bermuda petrel (Pterodroma cahow), and the relationship between female contaminant burden and breeding parameters. We found that petrels were exposed to a wide range of pollutants (33 out of 55 showed measurable levels) with PCBs dominating the blood contaminant profiles in both years. Only 9 compounds were detected in >50 % of the birds. Specifically, among OCPs, p, p'-DDE and hexaclorobenzene were the most frequently detected while fluorene and acenaphthene were the most common PAH. The concentrations of ∑5PCBs and ∑7POPs were higher in older birds. Furthermore, females with greater contaminant burdens laid eggs with a lower probability of hatching. However, female investment in egg production (size and volume) was unrelated to their blood contaminant load. Overall, this study highlights the presence of a wide range of contaminants in the petrel's food web, and it sheds light on the potential impact of chronic exposure to sub-lethal levels of PCBs on the breeding success of seabirds. We claim that toxicological testing should be a practice integrated in the management of seabirds, particularly of endangered species to monitor how past and present anthropogenic activities impact their conservation status.

Optimization and uncertainty assessment of a gas chromatography coupled to Orbitrap mass spectrometry method to determine organic contaminants in blood: A case study of an endangered seabird.

Birds are excellent bioindicators of environmental pollution, and blood provides information on contaminant exposure, although its analysis is challenging because of the low volumes that can be sampled. The objective of the present study was to optimize and validate a miniaturized and functional extraction and analytical method based on gas chromatography coupled to Orbitrap mass spectrometry (GCOrbitrap-MS) for the trace analysis of contaminants in avian blood. Studied compounds included 25 organochlorine pesticides (OCPs), 6 polychlorinated biphenyls (PCBs), 8 polybrominated diphenyl ethers (PBDEs) and 15 polycyclic aromatic hydrocarbons (PAHs). Four extraction and clean-up conditions were optimized and compared in terms of efficiency, accuracy, and uncertainty assessment. Extraction with hexane:dichloromethane and miniaturized Florisil pipette clean-up was the most adequate considering precision and accuracy, time, and costs, and was thereafter used to analyse 20 blood samples of a pelagic seabird, namely the Bermuda petrel (Pterodroma cahow). This species, endemic to the Northwest Atlantic, is among the most endangered seabirds of the region that in the '60 faced a decrease in the breeding success likely linked to a consistent exposure to dichloro-diphenyl-trichloroethane (DDT). Indeed, p,p'-DDE, the main DDT metabolite, was detected in all samples and ranged bewteen 1.13 and 6.87 ng/g wet weight. Other ubiquitous compounds were PCBs (ranging from 0.13 to 6.76 ng/g ww), hexachlorobenzene, and mirex, while PAHs were sporadically detected at low concentrations, and PBDEs were not present. Overall, the extraction method herein proposed allowed analysing very small blood volumes (∼ 100 µL), thus respecting ethical principles prioritising the application of less-invasive sampling protocols, fundamental when studying threatened avian species.

Global assessment of marine plastic exposure risk for oceanic birds.

Plastic pollution is distributed patchily around the world's oceans. Likewise, marine organisms that are vulnerable to plastic ingestion or entanglement have uneven distributions. Understanding where wildlife encounters plastic is crucial for targeting research and mitigation. Oceanic seabirds, particularly petrels, frequently ingest plastic, are highly threatened, and cover vast distances during foraging and migration. However, the spatial overlap between petrels and plastics is poorly understood. Here we combine marine plastic density estimates with individual movement data for 7137 birds of 77 petrel species to estimate relative exposure risk. We identify high exposure risk areas in the Mediterranean and Black seas, and the northeast Pacific, northwest Pacific, South Atlantic and southwest Indian oceans. Plastic exposure risk varies greatly among species and populations, and between breeding and non-breeding seasons. Exposure risk is disproportionately high for Threatened species. Outside the Mediterranean and Black seas, exposure risk is highest in the high seas and Exclusive Economic Zones (EEZs) of the USA, Japan, and the UK. Birds generally had higher plastic exposure risk outside the EEZ of the country where they breed. We identify conservation and research priorities, and highlight that international collaboration is key to addressing the impacts of marine plastic on wide-ranging species.

No evidence of inbreeding depression despite a historical severe bottleneck in the endangered Bermuda petrel (Pterodroma cahow).

The Bermuda petrel Pterodroma cahow is an island endemic seabird that belongs to the Procellariiformes, one of the most endangered orders of birds. Historical records suggest a significant population size decline following human settlement in Bermuda, bringing the species to near extinction. Since the 1950s, the population has been recovering aided by the implementation of an ongoing conservation plan. However, it still faces several threats, and negative genetic effects resulting from that drastic decline are to be expected, including inbreeding and genetic drift. We studied genetic diversity and levels of inbreeding, and their effects on individual fitness and mating choice. We also tested for a genetic signature of the recent demographic bottleneck. For this, we analyzed variation in thousands of nuclear single-nucleotide polymorphisms derived from double digest restriction site-associated DNA sequencing and 1 mitochondrial gene (cytochrome oxidase I). The results revealed that the Bermuda petrel suffered a recent genetic bottleneck and shows low mitochondrial diversity compared with other petrel species. Conversely, nuclear diversity was similar to that of other endangered petrels. Inbreeding levels were not high overall, although some individuals were highly inbred. However, we found no evidence that individual inbreeding or relatedness between mates affected hatching success, or that mate choice is influenced by kinship in this very small population.

Year-round variation in the isotopic niche of Scopoli's shearwater (Calonectris diomedea) breeding in contrasting sea regions of the Mediterranean Sea.

Top marine predators are key components of marine food webs. Among them, long-distance migratory seabirds, which travel across different marine ecosystems over the year, may experience important year-round changes in terms of oceanographic conditions and availability of trophic resources. We tested whether this was the case in the Scopoli's shearwater (Calonectris diomedea), a trans-equatorial migrant and top predator, by sampling birds breeding in three environmentally different regions of the Mediterranean Sea. The analysis of positional data and stable isotopes (δ1³C and δ15N) of target feathers revealed that birds from the three regions were spatially segregated during the breeding period while they shared non-breeding areas in the Atlantic Ocean. Isotopic baseline levels of N and C (meso-zooplankton) were significantly different among marine regions during breeding. Such variation was reflected at the higher trophic levels of pelagic and demersal fish muscles as well as in shearwater feathers grown in the Mediterranean. δ15N- and δ13C-adjusted values of shearwaters were significantly different among populations suggesting that birds from different breeding areas relied on prey species from different trophic levels. Conversely, the non-breeding spatial and isotopic niches overlapped greatly among the three populations. Shearwater trophic niches during breeding were narrower and segregated compared to the non-breeding period, revealing a high plasticity in trophic resource use. Overall, this study highlights seasonal and region-specific use of trophic resources by Scopoli's shearwater, suggesting a broad trophic plasticity and possibly a high adaptability to environmental changes.

Overlap between marine predators and proposed Marine Managed Areas on the Patagonian Shelf.

Static (fixed-boundary) protected areas are key ocean conservation strategies, and marine higher predator distribution data can play a leading role toward identifying areas for conservation action. The Falkland Islands are a globally significant site for colonial breeding marine higher predators (i.e., seabirds and pinnipeds). However, overlap between marine predators and Falkland Islands proposed Marine Managed Areas (MMAs) has not been quantified. Hence, to provide information required to make informed decisions regarding the implementation of proposed MMAs, our aims were to objectively assess how the proposed MMA network overlaps with contemporary estimates of marine predator distribution. We collated tracking data (1999-2019) and used a combination of kernel density estimation and model-based predictions of spatial usage to quantify overlap between colonial breeding marine predators and proposed Falkland Islands MMAs. We also identified potential IUCN Key Biodiversity Areas (pKBAs) using (1) kernel density based methods originally designed to identify Important Bird and Biodiversity Areas (IBAs) and (2) habitat preference models. The proposed inshore MMA, which extends three nautical miles from the Falkland Islands, overlapped extensively with areas used by colonial breeding marine predators. This reflects breeding colonies being distributed throughout the Falklands archipelago, and use being high adjacent to colonies due to central-place foraging constraints. Up to 45% of pKBAs identified via kernel density estimation were located within the proposed MMAs. In particular, the proposed Jason Islands Group MMA overlapped with pKBAs for three marine predator species, suggesting it is a KBA hot spot. However, tracking data coverage was incomplete, which biased pKBAs identified using kernel density methods, to colonies tracked. Moreover, delineation of pKBA boundaries were sensitive to the choice of smoothing parameter used in kernel density estimation. Delineation based on habitat model predictions for both sampled and unsampled colonies provided less biased estimates, and revealed 72% of the Falkland Islands Conservation Zone was likely a KBA. However, it may not be practical to consider such a large area for fixed-boundary management. In the context of wide-ranging marine predators, emerging approaches such as dynamic ocean management could complement static management frameworks such as MMAs, and provide protection at relevant spatiotemporal scales.

Trace elements' reference levels in blood of breeding black-browed albatrosses Thalassarche melanophris from the Falkland Islands.

Trace elements' concentration in the ocean is fast growing and is a source of major concern. Being charismatic and at the top of food chains, seabirds are often used as biological monitors of contaminants. We studied the concentration of trace elements in blood of black-browed albatross from the Falklands Islands, which we here show, by tracking with geolocators, forage over most of the Patagonian Shelf. Levels of trace elements were measured in males and females from two different islands. Blood concentrations of trace elements were not significantly different between islands, which is consistent with observations from foraging behavior revealing that birds from both islands foraged in broadly the same areas in the months before sampling. Arsenic and selenium concentrations in females were higher than in males. Sex-related differences in the concentration of these elements may be related to unknown slight differences in diet or to differences in assimilation between sexes. These results provide reference values for monitoring elemental contamination in the Patagonian Shelf Large Marine Ecosystem using black-browed albatrosses, one of the most abundant top predators and a suitable sentinel for the region's environmental health.

An ontogenetic perspective on migratory strategy of a long-lived pelagic seabird: Timings and destinations change progressively during maturation.

The processes that drive the ontogeny of migratory strategies in long-lived animals with slow maturation remain enigmatic. While some short-lived migrants are known or believed to repeat the same migratory patterns throughout their lives, little is known on the time required for immature long-lived migrants to progressively acquire adult-like migratory behaviours, or which aspects take longer to refine during the maturation process. Here, we studied the ontogeny of long-distance migratory strategies and related patterns of spatial distribution in a long-lived seabird species during the annual cycle. To do so, we deployed light-level geolocators on 4- to 9-year-old immature Cory's shearwaters (Calonectris borealis) and on breeding adults. We revealed that migratory timings and destinations of young shearwaters progressively changed with age. The effect of ageing was remarkably evident on spring migratory performance and phenology. Birds gradually shortened the duration of the non-breeding period by advancing departure date and reducing travelling time, which resulted in a sequential arrival at the colony of the various age contingents. Ageing immatures gradually changed from a more exploratory strategy to a more conservative way of exploiting resources, reducing both their year-round spatial spread across oceanic domains and the total distance travelled. Immatures always performed a trans-equatorial migration to the Southern Hemisphere, contrasting with 17% of the adults which remained in the North Atlantic year-round. Finally, during the breeding season immatures were widely dispersed through the North Atlantic reducing their overlap with breeding adults. Our long-term study provides empirical support to the hypothesis that in long-lived species, the refinement of migratory behaviour and year-round spatial distribution is a progressive process mediated by age and experience, where life stage constraints and competition for resources may also play a role. The emerging pattern suggests that for some avian taxa, the ontogeny of migratory strategy is a prolonged, complex and dynamic process.

Author Correction: Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

The Patagonian Shelf Large Marine Ecosystem supports high levels of biodiversity and endemism and is one of the most productive marine ecosystems in the world. Despite the important role marine predators play in structuring the ecosystems, areas of high diversity where multiple predators congregate remains poorly known on the Patagonian Shelf. Here, we used biotelemetry and biologging tags to track the movements of six seabird species and three pinniped species breeding at the Falkland Islands. Using Generalized Additive Models, we then modelled these animals' use of space as functions of dynamic and static environmental indices that described their habitat. Based on these models, we mapped the predicted distribution of animals from both sampled and unsampled colonies and thereby identified areas where multiple species were likely to overlap at sea. Maximum foraging trip distance ranged from 79 to 1,325 km. However, most of the 1,891 foraging trips by 686 animals were restricted to the Patagonian Shelf and shelf slope, which highlighted a preference for these habitats. Of the seven candidate explanatory covariates used to predict distribution, distance from the colony was retained in models for all species and negatively affected the probability of occurrence. Predicted overlap among species was highest on the Patagonian Shelf around the Falkland Islands and the Burdwood Bank. The predicted area of overlap is consistent with areas that are also important habitat for marine predators migrating from distant breeding locations. Our findings provide comprehensive multi-species predictions for some of the largest marine predator populations on the Patagonian Shelf, which will contribute to future marine spatial planning initiatives. Crucially, our findings highlight that spatially explicit conservation measures are likely to benefit multiple species, while threats are likely to impact multiple species.

Absence of haemosporidian parasite infections in the long-lived Cory's shearwater: evidence from molecular analyses and review of the literature.

The apparent scarcity or absence of blood parasites in some avian groups, such as seabirds, has been related to intrinsic and extrinsic factors including host immunological capacity, host-parasite assemblage, and ecological parameters, but also to reduced sensitivity of some methods to detect low parasite prevalence/intensities of infection. Here, we examined the haemosporidian parasite prevalence in a breeding population of Cory's shearwater Calonectris diomedea borealis, a long-distance migrant seabird, nesting in the Macaronesian region, in the Eastern Atlantic. Previous studies on Calonectris diomedea complex were based on small sample sizes providing weak evidence for a lack of infections by haemoparasites. Here, we investigated the presence of both parasite infections in C. d. borealis and larvae of potential mosquito vectors on the area. By employing a PCR-based assay, we extensively examined the prevalence of blood parasites belonging to the genera Plasmodium, Haemoproteus, and Leucocytozoon in 286 individuals from different life stages (i.e., chicks, immatures, sabbatical, and breeding adults), facing their specific energetic trade-offs (immunological functions vs. life history activities). We sampled immatures and adult shearwaters, of different sexes, ages, and migratory origins, from two sub-colonies. None of the sampled individuals were infected by these parasites, supporting the hypothesis that there was no in situ or ex situ transmission of vector-borne parasites in marine habitats irrespective of host's life stage and in spite of the presence of the potential Plasmodium vector Culiseta longiareolata breeding in the area. These results suggest that the lack of transmission of haemosporidian parasites on Selvagem Grande may be related to the lack of suitable dipteran vectors at the study sites, which may result from the geographic isolation of this area.

Quantifying space use of breeders and floaters of a long-lived species using individual movement data.

To date, animal movement studies have mostly analysed the movement behaviours of individuals at specific times of their lives, but we lack detailed information on how individual movements may be affected by the various and different changes that individuals experience throughout their life (e.g. life history phases, experience, age). Here, we attempt to identify differences in home range and movement behaviour between two different statuses, disperser vs. breeder, of a long-lived species (the eagle owl Bubo bubo). Information on home range and movement behaviour between different stages of an individual life are crucial for species conservation and management, as well as for basic knowledge on space use and rhythm of activity. Does the transition from an exploratory stage to moving within more familiar surroundings call for changes in the movement behaviour? We observed notable differences during the two stages of the owls' lives, with individuals having different home range behaviours and rhythms of activity depending on their social status. Significant differences in home range behaviour between the sexes began only with the acquisition of a breeding site. Breeders showed larger home ranges than dispersing individuals, although nightly variation of home ranges size was higher for dispersers than for breeders. Finally, dispersers were active throughout the night, whereas breeders displayed a less active movement phase at both the beginning and end of the night. Our results demonstrate it is important to consider individual variations in space use and movement behaviour due to the different life history phases that they attain during their lifetime. The knowledge of the different needs of a species across life stages may represent an important tool for species conservation because each phase of an individual life may need different requirements.

Population characteristics may reduce the levels of individual call identity.

Individual variability influences the demographic and evolutionary dynamics of spatially structured populations, and conversely ecological and evolutionary dynamics provide the context under which variations at the individual level occur. Therefore, it is essential to identify and characterize the importance of the different factors that may promote or hinder individual variability. Animal signaling is a prime example of a type of behavior that is largely dependent on both the features of individuals and the characteristics of the population to which they belong. After 10 years studying the dynamics of a population of a long-lived species, the eagle owl (Bubo bubo), we investigated the emergence and maintenance of traits that reveal individual identity by focusing on vocal features. We found that individuals inhabiting a high density population characterized by a relative lack of heterogeneity (in terms of prey availability and breeding success) among breeding sites might be selected for reducing the levels of identity. Two non-mutually exclusive hypotheses may explain the structural call patterns we detected: (1) similarity in calls may be principally a consequence of the particular characteristics of the population; and (2) high density may encourage individuals to mimic each other's vocalizations in a cascade effect, leading to a widespread and unique communication network.

Responses of a top and a meso predator and their prey to moon phases.

We compared movement patterns and rhythms of activity of a top predator, the Iberian lynx Lynx pardinus, a mesopredator, the red fox Vulpes vulpes, and their shared principal prey, the rabbit Oryctolagus cuniculus, in relation to moon phases. Because the three species are mostly nocturnal and crepuscular, we hypothesized that the shared prey would reduce its activity at most risky moon phases (i.e. during the brightest nights), but that fox, an intraguild prey of lynx, would avoid lynx activity peaks at the same time. Rabbits generally moved further from their core areas on darkest nights (i.e. new moon), using direct movements which minimize predation risk. Though rabbits responded to the increased predation risk by reducing their activity during the full moon, this response may require several days, and the moon effect we observed on the rabbits had, therefore, a temporal gap. Lynx activity patterns may be at least partially mirroring rabbit activity: around new moons, when rabbits moved furthest and were more active, lynxes reduced their travelling distances and their movements were concentrated in the core areas of their home ranges, which generally correspond to areas of high density of rabbits. Red foxes were more active during the darkest nights, when both the conditions for rabbit hunting were the best and lynxes moved less. On the one hand, foxes increased their activity when rabbits were further from their core areas and moved with more discrete displacements; on the other hand, fox activity in relation to the moon seemed to reduce dangerous encounters with its intraguild predator.

Individual and spatio-temporal variations in the home range behaviour of a long-lived, territorial species.

Despite the fact that investigations of home range behaviour have exponentially evolved on theoretical, analytical and technological grounds, the factors that shape animal home range behaviour still represent an unsolved question and a challenging field of research. However, home range studies have recently begun to be approached under a new integrated conceptual framework, considering home range behaviour as the result of the simultaneous influences of temporal, spatial and individual-level processes, with potential consequences at the population level. Following an integrated approach, we studied the influence of both external and internal factors on variations in the home range behaviour of 34 radiotagged eagle owl (Bubo bubo) breeders. Home range behaviour was characterised through complementary analysis of space use, movement patterns and rhythms of activity at multiple spatio-temporal scales. The effects of the different phases of the biological cycle became considerably evident at the level of movement patterns, with males travelling longer distances than females during incubation and nestling periods. Both external (i.e. habitat structure and composition) and internal (i.e. sex and health state) factors explained a substantial amount of the variation in home range behaviour. At the broader temporal scale, home range and core area size were negatively correlated with landscape heterogeneity. Males showed (1) smaller home range and core area sizes, (2) more complex home range internal structure and (3) higher rates of movement. The better the physiological condition of the individuals, the simpler the internal home range structure. Finally, inter- and intra-individual effects contributed to shaping space use and movement patterns during the biological cycle. Because of the plurality of behavioural and ecological processes simultaneously involved in home range behaviour, we claim that an integrative approach is required for adequate investigation of its temporal and spatial variation.

Moonlight makes owls more chatty.

BACKGROUND: Lunar cycles seem to affect many of the rhythms, temporal patterns and behaviors of living things on Earth. Ambient light is known to affect visual communication in animals, with the conspicuousness of visual signals being largely determined by the light available for reflection by the sender. Although most previous studies in this context have focused on diurnal light, moonlight should not be neglected from the perspective of visual communication among nocturnal species. We recently discovered that eagle owls Bubo bubo communicate with conspecifics using a patch of white throat plumage that is repeatedly exposed during each call and is only visible during vocal displays. METHODOLOGY/PRINCIPAL FINDINGS: Here we provide evidence that this species uses moonlight to increase the conspicuousness of this visual signal during call displays. We found that call displays are directly influenced by the amount of moonlight, with silent nights being more frequent during periods with no-moonlight than moonlight. Furthermore, high numbers of calling bouts were more frequent at moonlight. Finally, call posts were located on higher positions on moonlit nights. CONCLUSIONS/SIGNIFICANCE: Our results support the idea that moon phase affects the visual signaling behavior of this species, and provide a starting point for examination of this method of communication by nocturnal species.