Large-scale movements in the oceanic environment identify important foraging areas for loggerheads in central Mediterranean Sea

Loggerhead sea turtles (Caretta caretta) are known to display a wide range of movement patterns during the different stages of their life cycle, but empirical information to document this extensive behavioural plasticity is still limited. This is especially true for large, adult-sized individuals, that are thought to mainly forage in neritic areas. In the present paper, eight adult-sized loggerhead turtles were tracked using satellite telemetry to identify the location of their foraging grounds in the seas along the western coast of the Italian peninsula. Tracked turtles mostly stayed in the region between the Italian peninsula and the islands of Sicily and Sardinia, that was reached following quick, directed movements by the turtles from a release site to the north. In this area, two turtles took up residence in spatially limited neritic sites along the coast, while the remaining six alternated circumscribed coastal stays with long-distance, circuitous movements in the oceanic environment. An utilization distribution analysis clearly identified an area, mostly comprising oceanic waters, that was continuously used by turtles in different seasons and years. The present results contribute to the still-limited knowledge of the spatial ecology of loggerheads frequenting the Western Mediterranean Sea and highlight the presence of a potentially important oceanic region in the Southern Tyrrhenian Sea where adult-sized turtles forage for extended periods. These findings increase our knowledge of complex life history traits of loggerhead turtles and provide important information to be considered for evidence-based conservation measures

Living between widely separated areas: Long-term monitoring of Mediterranean loggerhead turtles sheds light on cryptic aspects of females spatial ecology

Over the last decades, satellite tracking techniques have substantially advanced our understanding of sea turtle spatial behaviour, especially for the post-nesting migrations of females. Substantial gaps remains in our knowledge of the turtle behaviour during the remaining inter-reproductive period, that spans over 2–3 years. We report the results of a prolonged tracking experiment on loggerhead turtles nesting along the Ionian Calabria, the main breeding ground in Italy. Argos satellite transmitters were deployed on eight females, a sample representing a substantial fraction of the overall population (20–25 nesting females). All turtles but one were tracked for > 300 days (range: 313–1523 days), revealing their spatial behaviour during a complete reproductive cycle and providing novel information on a number of poorly-known aspects of loggerhead spatial ecology: i) the post-nesting migratory strategy resulted in accordance with that of most adult loggerheads tracked so far, as the nine routes of six turtles were directed towards specific sites all located in the Tunisian continental shelf, a main foraging area for Mediterranean turtles; ii) the pre-breeding migratory routes were rather variable, likely deriving from different navigational strategies adopted by migrating turtles, and their temporal pattern indicates that mating occurred away from the nesting area; iii) the 10 inter-nesting movements of four turtles revealed unusual long-distance loops mostly in oceanic waters (median of maximum distance from nesting location: 145.5 km); iv) while at the foraging grounds, four turtles occupied distinct areas during summer and winter, making directed movements between the two sites, seasonal core areas were separated and their size was larger in winter than in summer (median: 498 km2 vs. 258 km2); v) individual females displayed an high fidelity to both sites in successive years. These findings further highlight the plasticity in loggerhead spatial behaviour and the importance of the Central Mediterranean and of the Tunisian shelf for loggerhead conservation

Testing a novel aggregated methodology to assess hydrodynamic impacts on a high-resolution marine turtle trajectory

We designed a novel aggregated methodology to infer the impact of ocean motions on the movements of satellite-tracked marine turtles adopting available oceanographic observations and validated products of a numerical oceanographic forecasting system. The method was tested on an 11-months trajectory of a juvenile loggerhead turtle (LT) wandering in the Tyrrhenian Sea (Mediterranean Sea) that was reconstructed with a high-resolution GPS tracking system. The application of ad-hoc designed metrics revealed that the turtle's route shape, ground speed and periodicities of its explained variance mimic the inertial motions of the sea, showing that this methodology is able to reveal important details on the relation between turtle movements and oceanographic features. Inertial motions were also identified in the observed trajectory of a surface drifting buoy sampling the Tyrrhenian Sea in a common period. At each sampling point of the turtle trajectory, the sea current eddy kinetic energy (EKE) and a Sea Current Impact index were computed from a validated set of high-resolution ocean modeling products and their analysis showed the relevant effects of the highly variable local sea currents mechanical action. Specifically, the metric we adopted revealed that the turtle trajectory was favorably impacted by the encountered sea current advection for about 70% of its length. The presented oceanographic techniques in conjunction with high-resolution tracking system provide a practicable approach to study marine turtle movements, leading the way to discover further insights on turtle behavior in the ocean

Assessing reliance on vector navigation in the long-distance oceanic migrations of green sea turtles

Vector navigation, i.e., maintaining a constant heading for a given amount of time, is hypothesized to provide a viable basis for the navigational feats of a number of long-distance animal migrants. Since animals following this strategy are subject to drift by wind or by ocean current, performing long migrations relying on vector navigation is particularly challenging. We tested whether vector navigation could be involved in the migrations of green turtles (Chelonia mydas) that migrate between the remote Ascension Island and Brazil. To this aim, a novel approach was followed using individual-based numerical models to simulate migratory trajectories of virtual turtles that were compared to actual routes reconstructed by satellite. Simulated postnesting migrations from Ascension revealed that weak currents enabled modeled turtles to reach the Brazilian coast, but only for a limited range of headings around due West. This conclusion was corroborated by comparing modeled trajectories with the actual routes of previously tracked turtles, with a beeline vector navigation strategy providing the best fit, although a true-navigation strategy directed to the landfall site produced similar results. Finally, we tested if a vector navigational strategy was feasible for the prebreeding migration from Brazil towards Ascension, but modeled routes mostly failed to reach the island or a larger area around it, with individuals drifting away under the influence of currents. We conclude that Ascension turtles can take advantage of vector navigation when migrating towards a wide target like the Brazilian coast, while the demanding prebreeding migration likely requires more complex navigational systems

Productivity changes in the Mediterranean Sea drive foraging movements of yelkouan shearwater Puffinus yelkouan from the core of its global breeding range

Pelagic seabirds are tied to their breeding colonies throughout their long-lasting breeding season, but at the same time, they have to feed in a highly dynamic marine environment where prey abundance and availability rapidly change across space and seasons. Here, we describe the foraging movements of yelkouan shearwater Puffinus yelkouan, a seabird endemic to the Mediterranean Sea that spends its entire life cycle within this enclosed basin and whose future conservation is intimately linked to human-driven and climatic changes affecting the sea. The aim was to understand the main factors underlying the choice of foraging locations during the reproductive phases. A total of 34 foraging trips were obtained from 21 breeding adults tagged and tracked on Tavolara Archipelago (N Sardinia, Italy). This is the largest and most important breeding area for the species, accounting for more than 50% of the world population. The relationships between foraging movements during two different breeding stages and the seasonal changes of primary productivity at sea were modeled. Movements appeared to be addressed toward inshore (<20 km), highly productive, and relatively shallow (<200 m) foraging areas, often in front of river mouths and at great distances from the colony. During incubation, the Bonifacio Strait and other coastal areas close to North and West Sardinia were the most preferred locations (up to 247 km from the colony). During the chick-rearing phase, some individuals reached areas placed at greater distances from the colony (up to 579 km), aiming at food-rich hotspots placed as far north as the Gulf of Lion (France). The need for such long distance and long-lasting foraging trips is hypothesized to be related to unfavorable conditions on the less productive (and already depleted) Sardinian waters

Inter and intra-population variability of the migratory behaviour of a short-distance partial migrant, the Eurasian Stone-curlew Burhinus oedicnemus (Charadriiformes, Burhinidae)

Migratory behaviour in birds shows a remarkable variability at species, population and individual levels. Short-distance migrants often adopt a partial migratory strategy and tend to have a flexible migration schedule that allows a more effective response to extreme environmental variations. Weather seasonality and environmental heterogeneity have been reported as significant factors in the diversification of migratory behaviour for Mediterranean migrants, but relatively few studies investigated the migration patterns of non-passerine birds migrating within the Mediterranean basin. In this study, we investigated the migratory strategy of 40 Eurasian Stone-curlews Burhinus oedicnemus tagged with geolocators and GPS-GSM tags and belonging to continental and Mediterranean populations of the Italian peninsula. The proportion of migrants was higher in continental populations, but we observed a significant variability also within Mediterranean populations. All birds spent the winter within the Mediterranean basin. Continental Stone-curlews departed earlier in spring and later in autumn and covered longer distances than those from Mediterranean areas. The speed of migration did not change between seasons for continental birds, while Mediterranean individuals migrated faster in spring. The likelihood of departure for autumn migration of GPS-tagged birds increased when temperatures were near or below 0 °C suggesting that Stone-curlews tend to delay departure until weather conditions worsen abruptly. As a consequence of global warming in the Mediterranean, the frequency of migratory birds in the considered populations might decrease in the near future. This could affect the distribution of species throughout the year and should be taken into account when targeting conservation measures

Comportamento migratorio e uso dello spazio in femmine di tartaruga comune

Riassunto La tartaruga comune è la specie di tartaruga marina più diffusa nel Mar Mediterraneo. Gli individui adulti vivono per la maggior parte del tempo in aree di foraggiamento in ambiente neritico, da cui le femmine ogni 2-3 anni si spostano verso le aree riproduttive, compiendo migrazioni anche a lunga distanza. Gli adulti mostrano una fedeltà sia alle zone di riproduzione che a quelle di alimentazione. Nel presente studio sono stati seguiti gli spostamenti di 6 femmine adulte nidificanti in Calabria applicando al loro carapace trasmittenti collegate al sistema satellitare Argos. Le tartarughe, marcate in anni diversi, sono state seguite per periodi compresi tra 5 e 36 mesi, per cui è stato possibile ricostruire i movimenti compiuti tra nidificazioni successive (periodo di internesting), le migrazioni post-riproduttive dirette alle aree di foraggiamento, i movimenti a breve scala compiuti durante il soggiorno nelle zone di foraggiamento e, per due individui, anche la migrazione pre-riproduttiva diretta verso le coste calabre. In questo modo sono stati definiti gli home range occupati nei siti di foraggiamento in Tunisia, cercando anche di interpretare i comportamenti degli animali in queste zone attraverso l’analisi di parametri ambientali rilevati nell’area ottenuti dal database online Movebank. Per ricostruire la rotta seguita dagli animali, i dati ottenuti da Argos sono stati filtrati per eliminare localizzazioni erronee e poco plausibili. Questo processo si è basato su criteri predeterminati che valutano le classi di accuratezza delle localizzazioni assegnate da Argos e la presenza di elevate velocità di spostamento tra localizzazioni successive, che risultino superiori a una soglia di velocità calcolata per ogni singolo individuo. Per determinare gli home range occupati dalle tartarughe nelle aree di foraggiamento sono state impiegate tecniche basate sul metodo Kernel con fattore di smussamento h ad hoc. A questo scopo, è stato utilizzato il pacchetto “adehabitat” del programma R. Infine, dopo aver identificato le due aree di foraggiamento annuali per ogni individuo, si sono confrontate le variabili ambientali (temperatura, batimetria, clorofilla, carbonio organico), che sono state rilevate nei due siti nello stesso periodo dell’anno. I risultati ottenuti mostrano che le tartarughe nidificanti in Calabria frequentano siti di foraggiamento individualmente specifici in ambiente neritico, localizzati lungo le coste tunisine, vicino al golfo di Gabés. La migrazione post-riproduttiva segue una rotta abbastanza lineare e diretta verso tali siti, mentre nelle migrazioni pre-riproduttive le tartarughe non raggiungono in modo diretto le coste calabre. Nei due casi studiati, una tartaruga ha prima raggiunto le coste siciliane, circumnavigando l’isola prima di fare rotta diretta verso la Calabria, mentre l’altra si è inizialmente spinta quasi fino in Grecia, per poi cambiare direzione e raggiungere le coste calabresi settentrionali, che poi ha costeggiato fino al sito di riproduzione. Nel periodo di internesting le tartarughe studiate hanno compiuto fino a 2-3 movimenti circolari in alto mare per ogni stagione riproduttiva. Nei siti di foraggiamento ciascuna tartaruga ha frequentato due aree principali, distanti circa 70 km tra loro, tra le quali si spostano sempre nello stesso periodo dell’anno. L’ampiezza degli home range occupati durante il soggiorno ai luoghi di foraggiamento tunisino è risultata differente tra i diversi individui studiati e il sito invernale è risultato generalmente più grande di quello estivo. Infine, l’analisi delle variabili ambientali ha rilevato come, sia in inverno che in estate, le tartarughe selezionino sempre l’area in cui la temperatura è più elevata, fornendo indicazioni sul ruolo della temperatura dell’acqua come elemento determinante nella scelta del sito di foraggiamento. Abstract Loggerhead sea turtles are widely distributed in the Mediterranean sea. Adults spend most of their time in neritic foraging grounds, from where they migrate towards their breeding areas every 2-3 years. Adults show a high fidelity to both their foraging sites and nesting beaches. In the present study we tracked through Argos satellite telemetry the movements of 6 adult female loggerheads nesting along the Calabrian Ionian coasts, in the south of Italy. The turtles were marked in different years and monitored for a period ranging from 5 to 36 months, and this allowed us to reconstruct the female movements during the inter-nesting period, the post nesting migration, their stay at foraging grounds and, for two animals, the pre-breeding migration back towards Calabria. We also estimated the turtles home ranges during their stay at the foraging grounds and examined the role of environmental parameters, obtained from Movebank databases, in determining the choice of the foraging grounds in different periods of the year. The data received from Argos have been filtered to exclude improbable locations and to reliably reconstruct the routes followed by the animals. To this aim we relied on a standard filtering process removing implausible locations determining movement speed exceeding a pre-determined speed threshold determined for each animal. Individual home ranges were calculated using Kernel methods with an h ad hoc, with the “adehabitat” package in the software R. Since each animal occupied two foraging sites during the year, we compared several environmental parameters (temperature, bathymetry, chlorophyll, organic carbon) between the two sites in the same period. The results show that during the post nesting migration all females followed a rather direct route towards their individually-specific, neritic foraging grounds located in the Tunisian shelf, near the Gulf of Gabès. Here each turtle occupied two different areas during the year, one in the winter season and one in spring-summer, with all females moving from one area to another in the same period. The pre-breeding migration tracked in two turtles was much less direct than the post nesting one: in one case the female first reached Sicily and then circumnavigated it to reach the Calabria nesting beaches, while the second turtle nearly reached Greece before changing her direction to reach Calabria’s northern coast. During the inter nesting period, tracked female carried out 2 or 3 long-distance loops in the high seas. The home range size at the foraging areas varied between animals, and three animals occupied larger home ranges during the winter than in summer. Finally, the comparison of environmental parameters in the two foraging sites showed that females chose to stay in the foraging ground with the highest sea surface temperature both in summer and during winter, providing indication for a role of water temperature in inducing turtles to move from a foraging area to another

The role of environmental factors on the spatial behaviour of three long-distance migratory species

Many vertebrate species embark in short or long migratory movements in order to make the most of the available resources. The animal’s decision on when to start and where to orient its movement is driven by an integration of the internal state of the individual with the external cues perceived: firstly, the migrant has to decide when is the right moment to start the migration in order to find good conditions along the route and at their final destination; and then it has to decide where to move, i.e. it has to orient towards the final goal. Apart from the central role played by the internal status of the animal in starting the migratory behaviour, the importance of external stimuli in influencing the final movement and route followed by the migrant, cannot be underestimated. Indeed, once the migration has started, environmental stimuli continue to have an effect on the animal movement by affecting the speed, accuracy and timing of migration, helping the individual in scheduling its arrival to the final destination (again related to the “when to move” issue) and influencing the actual path followed by the migrant (linked to the “where to move” problem). With the present thesis, I aimed at evaluating the role of environmental factors on the spatial behaviour of three migratory species: the European teal (Anas crecca), the loggerhead (Caretta caretta) and green sea turtle (Chelonia mydas) that were satellite tracked during their long-distance migrations. Teal data was used to answer the “when to go” question by assessing the influence of external cues on the onset of their spring migration. Conversely, sea turtle data was used to address the “where to go” issue investigating the turtles’ responses to the effect of sea currents during their migrations. Due to a general lack of information regarding teal migratory flyways in Europe, I firstly investigated teal migratory phenology by analysing tracking data of individuals wintering in three Italian sites. In this way I determined the course, speed and duration of their migratory movements, together with the number and length of stopovers made along the route. Most of the tracked teals left the wintering grounds between mid-February and March following a straight and direct route along the Black Sea-Mediterranean flyway, and reached the breeding sites located in North-Eastern Europe in May. Along their migratory route most birds stopped for several weeks at stopover sites, especially at the very beginning of migration, and this led to a slow overall migratory speed (36 km/d on average). Nevertheless, the active flight segments of the migration were covered at much higher speeds, up to 872 km/d. To correctly interpret the birds’ migratory strategy, it is crucial to properly identify the start of migration. Nevertheless, at present a univocal and objective method to assess the start of migration is missing, so I performed a comparative analysis between three different methods to determine the onset of migration using teal tracking data as an example. The starting dates identified by the tested methods were not always comparable, with the greatest inconsistencies among techniques being evident when the birds started early the migration and then stopped for a long period (>20 days) in a stopover area. This shows that caution is needed when choosing one technique over another, as the method used is likely to strongly affect any following analyses on migratory phenology. After having defined the migratory phenology of this species, I finally focused on investigating the effect of environmental cues on teal’s decision to start the migration. My analysis aimed at assessing if temperature and winds experienced during teal’s sojourn in an area could have had an effect on the decision to leave their wintering grounds and the site of the longest stopover, i.e. a stopover frequented at the beginning of migration for more than 20 days. I run two distinct Cox proportional models for wintering and the longest stopover area, including photoperiod as a control to determine if the models interpreted correctly the animal choices. As already noted for some goose species, the start of migration from the wintering ground was only triggered by the progressive increase of daylight hours, but, once the migration had started, the photoperiod lost its importance and teals took into consideration only the experienced temperatures to continue their migration from the longest stopover area. Winds experienced before departure, on the other hand, did not seem to play a role in teal’s decision to leave or not an area. The second part of my work addressed the “where to go” issue, specifically investigating the effect of sea currents on turtles during their open-sea migrations. Given that every swimming animal is affected by the flow of the medium it is moving in, the reconstructed route obtained from satellite-derived positions may not always be representative of the actual movement of the turtle and of its swimming speed. To assess the turtle’s active contribution to the tracked, ground-derived movement, I performed a vector subtraction between the ground-derived and sea currents velocities of three turtle populations migrating in quite different oceanographic conditions. The effect of sea currents along the turtle’s migratory routes was not homogeneous among populations, being greater in turtles migrating in the Indian Ocean than in those moving in the South Atlantic Ocean or in the Mediterranean Sea. These results thus highlight the importance of evaluating the sea currents encountered en-route by migrating turtles when studying their movements and inferring the behaviour, speed, etc. from tracking data. Deriving information on turtle’s migratory behaviour simply from tracking data and considering it representative of the actual active speed of the migrant, can indeed lead to errors, especially if the turtle is encountering strong and variable current fields along its route. The last aspect I investigated is strictly connected with the previous analysis, where it was observed that turtles nesting at Ascension Island and returning to the Brazilian coast at the end of their breeding season, mostly encountered weak currents flowing in the same direction of the turtle heading. This particular condition made me to hypothesise that this population could rely on a very simple navigational mechanism to reach their foraging grounds, like following a given direction for a certain amount of time (vector navigation). To test this hypothesis, I simulated the post- and pre-nesting migrations of turtles relying on different navigational strategies and, only for the post nesting migration, I compared the modelled turtle routes with the actual routes of turtles tracked. From the simulations obtained it was evident that the post nesting migrations towards a large target like the continental coast could indeed be performed following a simple vector strategy. The pre nesting migrations towards Ascension, instead, require a more complex system, like true navigation, given the difficulties in reaching such a small target located in the middle of the ocean. Thus, the navigation system of Ascension turtles could be another example of a coexistence of different navigational mechanisms in the same animal, that are used in different migrations to accomplish different orientation tasks

Evaluating vector navigation in green turtles migrating in a dynamic oceanic environment

It has been proposed that animals migrating towards a specific destination may rely on vector navigation by maintaining a direction for a certain amount of time. In sea turtles, reliance on this strategy has been proposed especially for migrations directed towards wide targets and carried out in weak sea current flows. In the present study we tested if vector navigation could also be a feasible strategy for turtles facing dynamic oceanographic conditions by considering the case of green turtles nesting in the Comoros archipelago and migrating to their foraging grounds along the African coast. To test this hypothesis, we firstly analysed the turtles’ actual headings estimated considering the currents encountered by migrating turtles along the open sea segment of their routes. We then run individual-based models to simulate the journeys of turtles migrating in the area while relying on a vector or a true navigation strategy, and reconstructed the turtle’s water-related, i.e. motor paths, by removing the drifting effect of sea currents. Tracked turtles did not show any major change in their headings and mostly oriented towards the foraging area. While simulations did not provide homogeneous results, the turtle orientation efficiency estimated from motor paths showed that they possibly relied on a vector rather than a true navigation strategy. The present results suggest that vector navigation is a viable strategy to account for the migratory performances recorded in turtles migrating in dynamic oceanographic conditions, even if the involvement of the more sophisticated true navigation mechanism cannot be completely excluded

Migratory restlessness and stopover duration in Wood sandpiper Tringa glareola

Factors affecting stopover duration in birds are still much discussed. Field studies report contradictory evidence regarding the effect of fuel reserves on bird decision to depart from a stopover site, while majority of laboratory tests performed on passerines reported a positive relationship between body conditions and migratory restlessness. In recent years, a few studies integrating laboratory and field investigations suggested that the amount of migratory restlessness could be a proxy of the individual willingness to depart from a stopover site in night-migrating passerines, but similar studies are lacking for other groups of birds. In this paper the factors affecting stopover length in the Wood sandpiper Tringa glareola (Charadriiformes Scolopacidae) were studied by integrating field observations and laboratory tests during spring migration. Our aims were to investigate (1) the influence of body conditions on migratory restlessness and (2) the influence of body conditions and of the amount of migratory restlessness on stopover duration, after controlling for meteorological conditions. Contrary to our expectations, we did not find any relationship between body condition and migratory restlessness nor stopover duration, while for the first time in a non-passerine species, evidence was produced that the amount of migratory restlessness is significantly related to the likelihood of leaving the stopover area. Our results emphasize the relevance of the studies integrating field and laboratory tests to understand the physiological and ecological factors affecting migration in different bird species