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  • Habitat preferences, foraging behaviour and bycatch risk among breeding sooty shearwaters Ardenna grisea in the Southwest Atlantic
    Publication . Bonnet-Lebrun, Anne-Sophie; Catry, Paulo; Clark, Tyler J.; Campioni, Letizia; Kuepfer, Amanda; Tierny, Megan; Kilbride, Elizabeth; Wakefield, Ewan D.
    Pelagic seabirds are important components of many marine ecosystems. The most abundant species are medium/small sized petrels (<1100 g), yet the sub-mesoscale (<10 km) distribution, habitat use and foraging behaviour of this group are not well understood. Sooty shearwaters Ardenna grisea are among the world’s most numerous pelagic seabirds. The majority inhabit the Pacific, where they have declined, partly due to bycatch and other anthropogenic impacts, but they are increasing in the Atlantic. To evaluate the sub-mesoscale habitat preferences (i.e. the disproportionality between habitat use and availability), diving behaviour and bycatch risk of Atlantic breeders, we tracked sooty shearwaters from the Falkland Islands during late incubation and early chick-rearing with GPS loggers (n = 20), geolocators (n = 10) and time-depth recorders (n = 10). These birds foraged exclusively in neritic and shelf-break waters, principally over the Burdwood Bank, ~350 km from their colony. Like New Zealand breeders, they dived mostly during daylight, especially at dawn and dusk, consistent with the exploitation of vertically migrating prey. However, Falkland birds made shorter foraging trips, shallower dives, and did not forage in oceanic waters. Their overlap with fisheries was low, and they foraged at shallower depths than those targeted by trawlers, the most frequent fishing vessels encountered, indicating that bycatch risk was low during late incubation/early chick-rearing. Although our results should be treated with caution, they indicate that Atlantic and Pacific sooty shearwaters may experience markedly differing pressures at sea. Comparative study between these populations, e.g. combining biologging and demography, is therefore warranted.
  • An ontogenetic perspective on migratory strategy of a long-lived pelagic seabird: Timings and destinations change progressively during maturation
    Publication . Letizia, Campioni; Dias, Maria P.; Granadeiro, José Pedro; Catry, Paulo
    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.
  • Absence of haemosporidian parasite infections in the long-lived Cory’s shearwater: evidence from molecular analyses and review of the literature
    Publication . Campioni, Letizia; Martínez-de la Puente, Josué; Figuerola, Jordi; Granadeiro, José P.; Silva, Mónica C.; Catry, Paulo
    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.
  • Trace elements’ reference levels in blood of breeding black-browed albatrosses Thalassarche melanophris from the Falkland Islands
    Publication . Furtado, Ricardo; Granadeiro, J. P.; Campioni, Letizia; Silva, Mónica; Pereira, Eduarda; Catry, Paulo
    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.
  • Important At-Sea areas of colonial breeding marine predators on the Southern Patagonian Shelf
    Publication . Baylis, Matthew; Tierney, Megan; Orben, Rachael; Evans, Victoria Warwick; Wakefield, Ewan; Grecian, William James; Trathan, Phil; Reisinger, Ryan R.; Ratcliffe, Norman Arthur; Croxall, John; Campioni, Letizia; Catry, Paulo; Crofts, Sarah; Boersma, P. Dee; Galimberti, Filippo; Granadeiro, José Pédro; Handley, Jonathan; Hayes, Sean; Hedd, April; Masello, Juan; Montevecchi, William A.; Pütz, Klemens; Quillfeldt, Petra; Rebstock, Ginger A.; Sanvito, Simona; Staniland, Iain; Brickle, Paul
    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.
  • Coastal connectivity of marine predators over the Patagonian Shelf during the highly pathogenic avian influenza outbreak
    Publication . Riaz, Javed; Orben, Rachael; Gamble, Amandine; Catry, Paulo; Granadeiro, Carlos; Campioni, Letizia; Tierney, Megan; Baylis, Alastair
    Animal movement and population connectivity are key areas of uncertainty in efforts to understand and predict the spread of infectious disease. The emergence of highly pathogenic avian influenza (HPAI) in South America poses a significant threat to globally significant populations of colonial breeding marine predators in the South Atlantic. Yet, there is a poor understanding of which species or migratory pathways may facilitate disease spread. Compiling one of the largest available animal tracking datasets in the South Atlantic, we examine connectivity and inter-population mixing for colonial breeding marine predators tagged at the Falkland Islands. We reveal extensive connectivity for three regionally dominant and gregarious species over the Patagonian Shelf. Black-browed albatrosses (BBA), South American fur seals (SAFS) and Magellanic penguins (MAG) used coastal waters along the Atlantic coast of South America (Argentina and Uruguay). These behaviours were recorded at or in close proximity to breeding colonies and haul-out areas with dense aggregations of marine predators. Transit times to and from the Falkland Islands to the continental coast ranged from 0.2–70 days, with 84% of animals making this transit within 4 days - a conservative estimate for HPAI infectious period. Our findings demonstrate BBA, SAFS and MAG connectivity between the Falkland Islands and mainland South America over an expansive spatial network and numerous pathways, which has implications for infectious disease persistence, transmission and spread. This information is vital in supporting HPAI disease surveillance, risk assessment and marine management efforts across the region.
  • A framework for mapping the distribution of seabirds by integrating tracking, demography and phenology
    Publication . Carneiro, Ana Paula B.; Pearmain, Elizabeth J.; Oppel, Steffen; Clay, Thomas A.; Phillips, Richard A.; Bonnet‐Lebrun, Anne‐Sophie; Wanless, Ross M.; Abraham, Edward; Richard, Yvan; Rice, Joel; Handley, Jonathan; Davies, Tammy E.; Dilley, Ben J.; Ryan, Peter G.; Small, Cleo; Arata, Javier; Arnould, John P. Y.; Bell, Elizabeth; Bugoni, Leandro; Letizia, Campioni; Catry, Paulo; Cleeland, Jaimie; Deppe, Lorna; Elliott, Graeme; Freeman, Amanda; Gonzalez-Solis, Jacob; Granadeiro, José Pedro; Grémillet, David; Landers, Todd J.; Makhado, Azwianewi; Nel, Deon; Nicholls, David G.; Rexer‐Huber, Kalinka; Robertson, Christopher J. R.; Sagar, Paul M.; Scofield, Paul; Stahl, Jean‐Claude; Stanworth, Andrew; Stevens, Kim L.; Trathan, Philip N.; Thompson, David R.; Torres, Leigh; Walker, Kath; Waugh, Susan M.; Weimerskirch, Henri; Dias, Maria P.
    1. The identification of geographic areas where the densities of animals are highest across their annual cycles is a crucial step in conservation planning. In marine environments, however, it can be particularly difficult to map the distribution of species, and the methods used are usually biased towards adults, neglecting the distribution of other life-history stages even though they can represent a substantial proportion of the total population. 2. Here we develop a methodological framework for estimating populationlevel density distributions of seabirds, integrating tracking data across the main life-history stages (adult breeders and non-breeders, juveniles and immatures). We incorporate demographic information (adult and juvenile/immature survival, breeding frequency and success, age at first breeding) and phenological data (average timing of breeding and migration) to weight distribution maps according to the proportion of the population represented by each life-history stage. 3. We demonstrate the utility of this framework by applying it to 22 species of albatrosses and petrels that are of conservation concern due to interactions with fisheries. Because juveniles, immatures and non-breeding adults account for 47%–81% of all individuals of the populations analysed, ignoring the distributions of birds in these stages leads to biased estimates of overlap with threats, and may misdirect management and conservation efforts. Population-level distribution maps using only adult distributions underestimated exposure to longline fishing effort by 18%–42%, compared with overlap scores based on data from all lifehistory stages. 4. Synthesis and applications. Our framework synthesizes and improves on previous approaches to estimate seabird densities at sea, is applicable for data-poor situations, and provides a standard and repeatable method that can be easily updated as new tracking and demographic data become available. We provide scripts in the R language and a Shiny app to facilitate future applications of our approach. We recommend that where sufficient tracking data are available, this framework be used to assess overlap of seabirds with at-sea threats such as overharvesting, fisheries bycatch, shipping, offshore industry and pollutants. Based on such an analysis, conservation interventions could be directed towards areas where they have the greatest impact on populations.
  • Overlap between marine predators and proposed Marine Managed Areas on the Patagonian Shelf
    Publication . Baylis, Alastair; Lecea, Ander M. De; Tierney, Megan; Orben, Rachael; Ratcliffe, Norman; Wakefield, Ewan; Catry, Paulo; Campioni, Letizia; Costa, Marina; Boersma, P. Dee; Galimberti, Filippo; Granadeiro, José P.; Masello, Juan; Puetz, Klemens; Quillfeldt, Petra; Rebstock, Ria; Sanvito, Simona; Staniland, Iain; Brickle, Paul
    Abstract. 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.
  • Colony attendance and moult pattern of Cory's Shearwaters (Calonectris borealis) differing in breeding status and age
    Publication . Campioni, Letizia; Roda, Sofia Bolumar; Alonso, Hany; Catry, Paulo; Granadeiro, José P.
    Migratory birds must fit three costly life-history events within the annual cycle, reproduction, moult and migration, to minimize their overlap and maximize survival and breeding success. However, some seabirds, such as Cory’s Shearwater Calonectris borealis, overlap body moult and breeding, with flight feather renewal occurring in late chick-rearing. In contrast, the moult patterns of non-breeding adult (sabbatical) and immature Cory’s Shearwaters, which also attend the colony during the breeding season, remain poorly understood. Furthermore, the potential implications of life-stage and breeding status trade-offs on moult status and colony attendance in non-breeders has rarely been investigated. Surveying different areas within one colony between June and September 2013 and 2014, we studied the age and breeding status composition of birds attending the breeding colony and scored moult of their body (breast and upper-neck), wing and tail feathers. We found that in addition to breeders (n = 165), 57.6% of the birds (n = 389) attending the colony were 4- to 10-year-old immatures (n = 132) and adult sabbatical shearwaters (n = 92). Sabbaticals and 8- to 10-year-old immatures (n = 28) were present at the colony during incubation, whereas only three sabbatical birds and no 8- to 10-year-old immatures were captured in late chick-rearing. Conversely, 4- to 7-year-old immatures arrived later in the season but were still present in late chick-rearing. Sabbatical and 8- to 10-year-old immatures were moulting body feathers at the same time as adult breeders, whereas, among 4- to 7-year-old immatures, older birds moulted earlier than younger birds. A larger proportion of sabbatical birds were replacing tail feathers compared with adult breeders. However, there was no evidence that sabbaticals or 8- to 10-year-old immatures differed in wing moult from adult breeders until August. Overall, our study shows that colony attendance by non-breeding adults and immatures is widespread in this population. The synchronous moult schedule of flight and body feathers across age groups at different life-history stages may suggest that this aspect of moult is controlled by environmental conditions.