Climate change drives migratory range shift via individual plasticity in shearwaters.

How individual animals respond to climate change is key to whether populations will persist or go extinct. Yet, few studies investigate how changes in individual behavior underpin these population-level phenomena. Shifts in the distributions of migratory animals can occur through adaptation in migratory behaviors, but there is little understanding of how selection and plasticity contribute to population range shift. Here, we use long-term geolocator tracking of Balearic shearwaters (Puffinus mauretanicus) to investigate how year-to-year changes in individual birds' migrations underpin a range shift in the post-breeding migration. We demonstrate a northward shift in the post-breeding range and show that this is brought about by individual plasticity in migratory destination, with individuals migrating further north in response to changes in sea-surface temperature. Furthermore, we find that when individuals migrate further, they return faster, perhaps minimizing delays in return to the breeding area. Birds apparently judge the increased distance that they will need to migrate via memory of the migration route, suggesting that spatial cognitive mechanisms may contribute to this plasticity and the resulting range shift. Our study exemplifies the role that individual behavior plays in populations' responses to environmental change and highlights some of the behavioral mechanisms that might be key to understanding and predicting species persistence in response to climate change.

Deep ocean drivers better explain habitat preferences of sperm whales Physeter macrocephalus than beaked whales in the Bay of Biscay.

Species Distribution Models are commonly used with surface dynamic environmental variables as proxies for prey distribution to characterise marine top predator habitats. For oceanic species that spend lot of time at depth, surface variables might not be relevant to predict deep-dwelling prey distributions. We hypothesised that descriptors of deep-water layers would better predict the deep-diving cetacean distributions than surface variables. We combined static variables and dynamic variables integrated over different depth classes of the water column into Generalised Additive Models to predict the distribution of sperm whales Physeter macrocephalus and beaked whales Ziphiidae in the Bay of Biscay, eastern North Atlantic. We identified which variables best predicted their distribution. Although the highest densities of both taxa were predicted near the continental slope and canyons, the most important variables for beaked whales appeared to be static variables and surface to subsurface dynamic variables, while for sperm whales only surface and deep-water variables were selected. This could suggest differences in foraging strategies and in the prey targeted between the two taxa. Increasing the use of variables describing the deep-water layers would provide a better understanding of the oceanic species distribution and better assist in the planning of human activities in these habitats.

First assessment of floating marine litter abundance and distribution in the Bay of Biscay from an integrated ecosystem survey.

In the Bay of Biscay, regional monitoring programmes and data on abundance and distribution of floating marine litter are scarce, contrary to many other European marine regions. Here, a joint analysis of multiyear observations (2017-2019) of floating micro and macrolitter and oceanographic conditions was conducted for the Bay of Biscay by combining microlitter samplings with neuston nets and vessel-based macrolitter observations. Results show spatiotemporal abundance and distribution patterns. The density of floating microlitter increased from 26,056 items/km2 in 2017 to 1,802,4611 items/km2 in 2019; floating macrolitter densities barely varied amongst year (2.52 items/km2 in 2017 and 3.70 items/km2 in 2019). No significant correlation was found between densities of micro and macrolitter, neither for the oceanographic variables. We conclude that longer micro and macrolitter monitoring periods and standardized datasets based on the cross-border cooperation are needed to collect more comparable information, evaluate trends, and support decision making in the area.

Towards a better characterisation of deep-diving whales' distributions by using prey distribution model outputs?

In habitat modelling, environmental variables are assumed to be proxies of lower trophic levels distribution and by extension, of marine top predator distributions. More proximal variables, such as potential prey fields, could refine relationships between top predator distributions and their environment. In situ data on prey distributions are not available over large spatial scales but, a numerical model, the Spatial Ecosystem And POpulation DYnamics Model (SEAPODYM), provides simulations of the biomass and production of zooplankton and six functional groups of micronekton at the global scale. Here, we explored whether generalised additive models fitted to simulated prey distribution data better predicted deep-diver densities (here beaked whales Ziphiidae and sperm whales Physeter macrocephalus) than models fitted to environmental variables. We assessed whether the combination of environmental and prey distribution data would further improve model fit by comparing their explanatory power. For both taxa, results were suggestive of a preference for habitats associated with topographic features and thermal fronts but also for habitats with an extended euphotic zone and with large prey of the lower mesopelagic layer. For beaked whales, no SEAPODYM variable was selected in the best model that combined the two types of variables, possibly because SEAPODYM does not accurately simulate the organisms on which beaked whales feed on. For sperm whales, the increase model performance was only marginal. SEAPODYM outputs were at best weakly correlated with sightings of deep-diving cetaceans, suggesting SEAPODYM may not accurately predict the prey fields of these taxa. This study was a first investigation and mostly highlighted the importance of the physiographic variables to understand mechanisms that influence the distribution of deep-diving cetaceans. A more systematic use of SEAPODYM could allow to better define the limits of its use and a development of the model that would simulate larger prey beyond 1,000 m would probably better characterise the prey of deep-diving cetaceans.

First days at sea: depicting migration patterns of juvenile seabirds in highly impacted seascapes.

Increasing human activities have detrimental consequences on marine ecosystems and their impact can have cumulative effects. Within marine ecosystems, seabirds respond to ecosystem variability and face multiple human pressures, especially threatened species. In long-lived species, juveniles and immatures could represent up to 50% of the total population, but their migratory movements remain largely unknown. Here, we depict the migratory patterns of juvenile Balearic shearwaters Puffinus mauretanicus, the most threatened European seabird, using miniaturised satellite transmitters. At the end of the 2012 breeding season, five tagged juveniles left the breeding colonies of Eivissa Island (western Mediterranean) the first week of July. They moved westwards to reach the Atlantic Ocean between 3 and 13 days afterwards. Juveniles showed a two-phase migratory pattern: they first travelled slower close to the breeding colonies, and then moved towards their wintering areas in the Atlantic Ocean by rapid directional movements. Environmental cues (e.g.,marine productivity, water mass distribution, frontal systems) might have a prominent role in driving the migratory patterns of juvenile Balearic shearwaters, moving from warm and poor marine areas in the Mediterranean Sea to cooler and rich non-breeding grounds in the Atlantic Ocean. Based on observational findings, we observed certain spatial overlap of juvenile Balearic shearwaters with areas of high human impact, but the relationship between flying travel speed and both fishing effort and cumulative human impacts were not statistically significant. These results suggest that more research is needed to assess whether the movement patterns of migrating juveniles are affected by human activities. Therefore, understanding the at-sea spatial ecology of juveniles should be a priority for research and conservation due to the importance of this population component in long-lived species, as well as assessing their vulnerability to multiple anthropogenic pressures.

Including ecosystem descriptors in current fishery data collection programmes to advance towards a holistic monitoring: Seabird abundance attending demersal trawlers.

To develop an ecosystem-based approach to fisheries management a holistic perspective is necessary that goes beyond target species management to preserve ecosystem functioning and, therefore, secure future food availability. To achieve these objectives, current fishery data collection programmes should widen their objectives to include the collection of ecosystem descriptors to effectively take advantage of funding and human resources in relation to fisheries monitoring already in place. From an ecological perspective, fishing discards are food subsidies unnaturally available that can profoundly impact the life history traits and population dynamics of seabirds, as well as community structure. In 2015, we took advantage of the Data Collection Framework (DCF) programme, monitoring the Basque trawling fleet, to monitor seabird abundance associated with trawlers as an additional task to be performed by the observers. The main objectives were (1) to develop a standard protocol from an interdisciplinary expert committee, (2) to obtain baseline information of seabird association with trawlers to be able to track changes and (3) to understand seabird abundance in relation to discard facilitation processes based on environmental and fishing parameters. Based on the developed standard protocol, more than 21 species of seabirds were recorded in 241 fishing hauls in the Bay of Biscay (ICES areas 8abd). This biogeographic area is an important migratory flyway and wintering area, where maximum number of seabirds attending trawlers were recorded between December and April (2015-2019). Based on Generalised Linear Models, seabird abundance was higher in multiple situations: harsher environmental conditions, less available discards, shallower areas, increased period of discard availability, higher number of trawlers simultaneously operating in the same fishing ground, in addition to the months of February and April. The core discarding ground was located in the outer French shelf between the latitudinal range of 44.5°N and 46°N, especially for otter trawl fishing. Our approach puts into value the seabird counts that the observers of the DCF can perform systematically, collecting relevant information on the effect of trawling on other biodiversity components such as seabirds. This information will be critical to respond to the application of the reform of the Common Fisheries Policy regarding the effect of the Landing Obligation that seeks fishing sustainability.

Spatio-temporal patterns of northern gannet abundance in a migratory and wintering area.

In marine ecosystems, seabird populations are well monitored, thus allowing their use as indicators of system fluctuations at multiple spatio-temporal scales. Population abundance estimates are essential features of any conservation and management measures and initiatives. Population abundances can be used to delineate the distribution range and foraging grounds of species during both breeding and non-breeding periods, with multi-annual monitoring allowing for the inspection of the temporal variability within key marine areas. Taking advantage of long-term monitoring schemes, we examined the annual abundance patterns of the northern gannet Morus bassanus in its southern European migratory flyway. Here, the presence of a topographical feature (i.e. a submarine canyon system) could influence physical processes (e.g. upwelling, alongshore currents, and riverine inputs), thus oceanographically differentiating canyon and shelf ecosystems within a spatially restricted marine area. We assessed seasonal and long-term trend fluctuations of monthly northern gannet abundance using Generalized Additive Mixed Models, yielding only a strong seasonal effect. Moreover, we jointly tested the effect of the phenology and the spatial domain (canyon versus shelf) on northern gannet abundance using Generalised Linear Mixed Models, accounting for the excess of zeros. Northern gannet abundance was higher during the pre-winter and post-winter migration, corresponding to its southward and northward movements in the NE Atlantic, respectively. The effect of the canyon was only detected during the post-winter migration. By age, adult northern gannets were more abundant in some periods of the year (from October to March, including the pre-winter migration, the wintering and the post-winter migration), whereas juveniles and immatures were especially abundant during the pre-winter period. Our results could provide quantitative baseline information of northern gannet spatio-temporal patterns in a migratory and wintering area important for both research and conservation efforts, given the high conservation value of the area within the Natura 2000 network.

Incidence of plastic ingestion in seabirds from the Bay of Biscay (southwestern Europe).

Seabirds have been widely used to monitor marine debris by the analysis of plastic ingestion. With the aim of obtaining the first data on ingestion of plastics by different seabird species in the Bay of Biscay and evaluating their suitability as biomonitors of plastic pollution in this area, a total of 159 seabirds of fifteen species were analyzed. Plastics were found in 26 birds (16% of the individuals) of nine species (60% of the species). Frequency of occurrence of plastics varied between 0% (Razorbill) and 100% (species of the family Procellariidae). Considering several criteria to assess their suitability as biomonitors of plastic pollution (frequency of occurrence of plastic ingestion, species abundances and stranding occurrence in the Bay of Biscay), the Common Guillemot and the Atlantic Puffin seem the most promising candidates. This study provides the first data on plastic ingestion in seabirds of the Bay of Biscay.

Can Static Habitat Protection Encompass Critical Areas for Highly Mobile Marine Top Predators? Insights from Coastal East Africa.

Along the East African coast, marine top predators are facing an increasing number of anthropogenic threats which requires the implementation of effective and urgent conservation measures to protect essential habitats. Understanding the role that habitat features play on the marine top predator' distribution and abundance is a crucial step to evaluate the suitability of an existing Marine Protected Area (MPA), originally designated for the protection of coral reefs. We developed species distribution models (SDM) on the IUCN data deficient Indo-Pacific bottlenose dolphin (Tursiops aduncus) in southern Kenya. We followed a comprehensive ecological modelling approach to study the environmental factors influencing the occurrence and abundance of dolphins while developing SDMs. Through the combination of ensemble prediction maps, we defined recurrent, occasional and unfavourable habitats for the species. Our results showed the influence of dynamic and static predictors on the dolphins' spatial ecology: dolphins may select shallow areas (5-30 m), close to the reefs (< 500 m) and oceanic fronts (< 10 km) and adjacent to the 100 m isobath (< 5 km). We also predicted a significantly higher occurrence and abundance of dolphins within the MPA. Recurrent and occasional habitats were identified on large percentages on the existing MPA (47% and 57% using presence-absence and abundance models respectively). However, the MPA does not adequately encompass all occasional and recurrent areas and within this context, we propose to extend the MPA to incorporate all of them which are likely key habitats for the highly mobile species. The results from this study provide two key conservation and management tools: (i) an integrative habitat modelling approach to predict key marine habitats, and (ii) the first study evaluating the effectiveness of an existing MPA for marine mammals in the Western Indian Ocean.

Combining Methods to Describe Important Marine Habitats for Top Predators: Application to Identify Biological Hotspots in Tropical Waters.

In tropical waters resources are usually scarce and patchy, and predatory species generally show specific adaptations for foraging. Tropical seabirds often forage in association with sub-surface predators that create feeding opportunities by bringing prey close to the surface, and the birds often aggregate in large multispecific flocks. Here we hypothesize that frigatebirds, a tropical seabird adapted to foraging with low energetic costs, could be a good predictor of the distribution of their associated predatory species, including other seabirds (e.g. boobies, terns) and subsurface predators (e.g., dolphins, tunas). To test this hypothesis, we compared distribution patterns of marine predators in the Mozambique Channel based on a long-term dataset of both vessel- and aerial surveys, as well as tracking data of frigatebirds. By developing species distribution models (SDMs), we identified key marine areas for tropical predators in relation to contemporaneous oceanographic features to investigate multi-species spatial overlap areas and identify predator hotspots in the Mozambique Channel. SDMs reasonably matched observed patterns and both static (e.g. bathymetry) and dynamic (e.g. Chlorophyll a concentration and sea surface temperature) factors were important explaining predator distribution patterns. We found that the distribution of frigatebirds included the distributions of the associated species. The central part of the channel appeared to be the best habitat for the four groups of species considered in this study (frigatebirds, brown terns, boobies and sub-surface predators).

Coupling instantaneous energy-budget models and behavioural mode analysis to estimate optimal foraging strategy: an example with wandering albatrosses.

BACKGROUND: How foragers move across the landscape to search for resources and obtain energy is a central issue in ecology. Direct energetic quantification of animal movements allows for testing optimal foraging theory predictions which assumes that animals forage so as to maximise net energy gain. Thanks to biologging advances, we coupled instantaneous energy-budget models and behavioural mode analysis to test optimal foraging theory predictions on wandering albatross Diomedea exulans during the brooding period. Specifically, the instantaneous energy-budget model considered the energetic balance (i.e., the difference between empirical energy gain data and modelled energy expenditure via heart rate values) along the trajectory of a given individual. Four stereotypic instantaneous behavioural modes were identified based on trajectory properties (e.g., speed and turning angle) by applying a new algorithm called Expectation Maximization Binary Clustering. Previous studies on this species have shown that foraging-in-flight is the optimal foraging strategy during the incubation period when albatrosses undertake long-distance movements but no specific foraging strategy has been determined for shorter foraging movements (e.g., brooding period). RESULTS: The output of our energy-budget model (measured as net energy gain) highlighted the potential optimality of alternative search strategies (e.g., sit-and-wait) during brooding, when birds may be subjected to specific energetic trade-offs and have to adapt their foraging strategies accordingly. However, not all birds showed this pattern, revealing the importance of considering individual variability in foraging strategies, as well as any switching among strategies, before drawing population-level generalizations. Finally, our study unveils the importance of considering fine scale activities to make realistic estimates of trip energy expenditure for flying birds at sea. CONCLUSIONS: The up-scaling of accurately measured fine-scale energy patterns is essential to quantify energy balances, and their fluctuations by season of different activities among individuals or populations. In particular, we offer new insights for the energetic quantification of the effect of changing oceanic winds on the biology of pelagic predators in the southern oceans.

Protecting persistent dynamic oceanographic features: transboundary conservation efforts are needed for the critically endangered Balearic shearwater.

The protection of key areas for biodiversity at sea is not as widespread as on land and research investment is necessary to identify biodiversity hotspots in the open ocean. Spatially explicit conservation measures such as the creation of representative networks of marine protected areas (MPAs) is a critical step towards the conservation and management of marine ecosystems, as well as to improve public awareness. Conservation efforts in ecologically rich and threatened ecosystems are specially needed. This is particularly urgent for the Mediterranean marine biodiversity, which includes highly mobile marine vertebrates. Here, we studied the at sea distribution of one of the most endangered Mediterranean seabird, the critically endangered Balearic shearwater Puffinus mauretanicus. Present knowledge, from vessel-based surveys, suggests that this species has a coastal distribution over the productive Iberian shelf in relation to the distribution of their main prey, small pelagic fish. We used miniaturised satellite transmitters to determine the key marine areas of the southern population of Balearic shearwaters breeding on Eivissa and spot the spatial connections between breeding and key marine areas. Our tracking study indicates that Balearic shearwaters do not only forage along the Iberian continental shelf but also in more distant marine areas along the North African coast, in particular W of Algeria, but also NE coast of Morocco. Birds recurrently visit these shelf areas at the end of the breeding season. Species distribution modelling identified chlorophyll a as the most important environmental variable in defining those oceanographic features characterizing their key habitats in the western Mediterranean. We identified persistent oceanographic features across time series available in the study area and discuss our results within the current conservation scenario in relation to the ecology of the species.

Changes in wind pattern alter albatross distribution and life-history traits.

Westerly winds in the Southern Ocean have increased in intensity and moved poleward. Using long-term demographic and foraging records, we show that foraging range in wandering albatrosses has shifted poleward in conjunction with these changes in wind pattern, while their rates of travel and flight speeds have increased. Consequently, the duration of foraging trips has decreased, breeding success has improved, and birds have increased in mass by more than 1 kilogram. These positive consequences of climate change may be temporary if patterns of wind in the southern westerlies follow predicted climate change scenarios. This study stresses the importance of foraging performance as the key link between environmental changes and population processes.

Fishery discards impact on seabird movement patterns at regional scales.

Human fishing activities are negatively altering marine ecosystems in many ways [1, 2], but scavenging animals such as seabirds are taking advantage of such activities by exploiting fishery discards [3-5]. Despite the well-known impact of fisheries on seabird population dynamics [6-10], little is known about how discard availability affects seabird movement patterns. Using scenarios with and without trawling activity, we present evidence that fisheries modify the natural way in which two Mediterranean seabirds explore the seascape to look for resources during the breeding season. Based on satellite tracking data and a mathematical framework to quantify anomalous diffusion phenomena, we show how the interplay between traveling distances and pause periods contributes to the spatial spreading of the seabirds at regional scales (i.e., 10-250 km). When trawlers operate, seabirds show exponentially distributed traveling distances and a strong site fidelity to certain foraging areas, the whole foraging process being subdiffusive. In the absence of trawling activity, the site fidelity increases, but the whole movement pattern appears dominated by rare but very large traveling distances, making foraging a superdiffusive process. Our results demonstrate human involvement on landscape-level behavioral ecology and provide a new ecosystemic approach in the study of fishery-seabird interactions.

Digit length may reveal unusual breeding behaviour in a seabird.

The hormonal environment experienced during prenatal development may affect adult phenotype and behaviour. Digit lengths may provide an estimate of steroid levels encountered during embryonic development in humans and other vertebrates. Finger patterns in humans have been shown to reveal sexual orientation or cooperative behaviour. We explored individual breeding behaviour in a monogamous seabird, the Balearic shearwater Puffinus mauretanicus and unexpectedly detected some cooperative breeders. Furthermore, we show evidence of correlation between digit lengths and cooperative breeding in this species. Additionally, we suggest that the first digit could be a possible indicator of prenatal steroid levels. These results are the starting point for further tests of the hypothesis that first digit length is an indicator of prenatal hormone levels in other vertebrate species. Moreover, these results may offer practical use in wild populations to study the implications of the changes in prenatal environment for adult social behaviour.

Living close, doing differently: small-scale asynchrony in demography of two species of seabirds.

Studies on spatiotemporal pattern of population abundance predict that close populations should exhibit a high level of synchrony, reflected in a parallel time variation of at least one demographic parameter. We tested this prediction for two threatened species of Procellariiformes sharing similar life history traits: the European Storm Petrel (Hydrobates pelagicus) and the Balearic Shearwater (Puffinus mauretanicus). Within each species, we compared adult survival, proportion of transients (breeders that do not settle), and average productivity at two neighboring colonies. Physical and environmental features (e.g., food availability) of the breeding sites were similar. However, while Balearic Shearwater colonies were free of predators, aerial predators occurred especially in one colony of the European Storm Petrel. Despite this difference, we found similar results for the two species. A high proportion of transient birds was detected in only one colony of each species, ranging between 0.00-0.38 and 0.10-0.63 for the petrels and shearwaters, respectively. This seems to be an emergent feature of spatially structured populations of seabirds, unrelated to colony size or predator pressure, that can have important demographic consequences for local population dynamics and their synchrony. Local survival of resident birds was different at each colony, an unexpected result, especially for predator-free colonies of Balearic Shearwater. Productivity varied between the two colonies of European Storm Petrels, but not between the two colonies of Balearic Shearwaters. We demonstrated that within each species, several demographic parameters were colony specific and sufficiently different to generate short-term asynchronous dynamics. Our findings suggest that, in spatially structured populations, local factors, such as predation or small-scale habitat features, or population factors, such as individual quality or age structure, can generate unexpected asynchrony between neighboring populations.

Oceanographic habitat of an endangered Mediterranean procellariiform: implications for marine protected areas.

Marine protected areas (MPAs) require ecologically meaningful designs capable of taking into account the particularities of the species under consideration, the dynamic nature of the marine environment, and the multiplicity of anthropogenic impacts. MPAs have been most often designated to protect benthic habitats and their biota. Increasingly, there is a need to account for highly mobile pelagic taxa, such as marine birds, mammals and turtles, and their oceanic habitats. For breeding seabirds foraging from a central place, particular attention should be paid to distant foraging grounds and movement corridors, which can often extend to hundreds of kilometers from breeding colonies. We assessed the habitat use by the most threatened Mediterranean seabird, the Balearic Shearwater, Puffinus mauretanicus, using vessel-based surveys during the chick-rearing period (May-June). We used a hierarchical modeling approach to identify those environmental variables that most accurately reflected the oceanographic habitat of this species by (1) delineating its foraging range using presence/ absence data and (2) identifying important foraging grounds where it concentrates in dense aggregations. The foraging range comprised the frontal systems along the eastern Iberian continental shelf waters (depth <200 m) and areas close to the breeding colonies in the Balearic Islands. Shearwaters aggregated in productive shelf areas with elevated chlorophyll a concentrations. Following the model of a core-buffer MPA, we envisioned those areas of dense aggregation (i.e., the area of influence of the Ebro River discharge and Cape La Nao regions) as the core regions deserving elevated protection and more stringent management. More diffuse protective measures would be applied within the larger buffer region, delineated by the foraging range of the species. Marine zoning measures can greatly benefit the conservation of the Balearic Shearwater and other far-ranging seabirds by extending protective measures beyond their breeding colonies during both the breeding and non-breeding seasons.