Beneath the Antarctic sea-ice: Fine-scale analysis of Weddell seal (Leptonychotes weddellii) behavior and predator-prey interactions, using micro-sonar data in Terre Adélie.

Lactation is the most energy-demanding event in mammals' reproduction. In pinnipeds, females are the only food providers to the young and have developed numerous behavioral and physiological lactation strategies, from capital-breeding to income-breeding. Lactating females' fine-scale foraging strategy, and precise understanding of how females supplement their pup's needs as well as their own are important to understand the species' ecology and energetic balance. Polar pinnipeds, inhabiting extreme environments, are sensitive to climate change and variability, understanding their constraints and foraging strategy during lactation is therefore important. In 2019, three sonar tags were deployed on lactating Weddell seals in Terre Adélie (East Antarctica) for 7 days, to study fine-scale predator-prey interactions. Feeding activity was mostly benthic, reduced, central-placed, and spatially limited. Females spent most of their time hauled-out. A total of 331 prey capture attempts (PrCAs) were recorded using triaxial acceleration data, with 125 prey identified on echograms (5 cm, acoustic size). All PrCAs occurred on the seafloor, shallower than usual records (mean depth of 88 m, vs 280 m after their molt). We also found that they only fed in three of the five identified dive shapes, during the ascent or throughout the dive. Half of the prey were reactive to the seal's approach, either leaving the seafloor, or escaping just above the seafloor, suggesting that the seals hunt by chasing them from the seabed. Seals continuously scanned the area during the approach phase, evoking opportunistic foraging. Our results provide additional evidence that Weddell seal forage during lactation, displaying a mix of capital-breeding and income-breeding strategies during this period of physiological stress. This work sheds light on previously unexplored aspects of their foraging behavior, such as shallow water environments, targeting benthic prey, generally focusing on single prey rather than schools, and evidence of visual scanning through observed head movements.

Decadal changes in blood δ13C values, at-sea distribution, and weaning mass of southern elephant seals from Kerguelen Islands.

Changes in the foraging environment and at-sea distribution of southern elephant seals from Kerguelen Islands were investigated over a decade (2004-2018) using tracking, weaning mass, and blood δ13C values. Females showed either a sub-Antarctic or an Antarctic foraging strategy, and no significant shift in their at-sea distribution was detected between 2004 and 2017. The proportion of females foraging in sub-Antarctic versus Antarctic habitats did not change over the 2006-2018 period. Pup weaning mass varied according to the foraging habitat of their mothers. The weaning mass of sub-Antarctic foraging mothers' pups decreased by 11.7 kg over the study period, but they were on average 5.8 kg heavier than pups from Antarctic foraging mothers. Pup blood δ13C values decreased by 1.1‰ over the study period regardless of their sex and the presumed foraging habitat of their mothers. Together, these results suggest an ecological change is occurring within the Indian sector of the Southern Ocean with possible consequences on the foraging performance of southern elephant seals. We hypothesize that this shift in δ13C is related to a change in primary production and/or in the composition of phytoplankton communities, but this requires further multidisciplinary investigations.

Tracking of marine predators to protect Southern Ocean ecosystems.

Southern Ocean ecosystems are under pressure from resource exploitation and climate change1,2. Mitigation requires the identification and protection of Areas of Ecological Significance (AESs), which have so far not been determined at the ocean-basin scale. Here, using assemblage-level tracking of marine predators, we identify AESs for this globally important region and assess current threats and protection levels. Integration of more than 4,000 tracks from 17 bird and mammal species reveals AESs around sub-Antarctic islands in the Atlantic and Indian Oceans and over the Antarctic continental shelf. Fishing pressure is disproportionately concentrated inside AESs, and climate change over the next century is predicted to impose pressure on these areas, particularly around the Antarctic continent. At present, 7.1% of the ocean south of 40°S is under formal protection, including 29% of the total AESs. The establishment and regular revision of networks of protection that encompass AESs are needed to provide long-term mitigation of growing pressures on Southern Ocean ecosystems.

The retrospective analysis of Antarctic tracking data project.

The Retrospective Analysis of Antarctic Tracking Data (RAATD) is a Scientific Committee for Antarctic Research project led jointly by the Expert Groups on Birds and Marine Mammals and Antarctic Biodiversity Informatics, and endorsed by the Commission for the Conservation of Antarctic Marine Living Resources. RAATD consolidated tracking data for multiple species of Antarctic meso- and top-predators to identify Areas of Ecological Significance. These datasets and accompanying syntheses provide a greater understanding of fundamental ecosystem processes in the Southern Ocean, support modelling of predator distributions under future climate scenarios and create inputs that can be incorporated into decision making processes by management authorities. In this data paper, we present the compiled tracking data from research groups that have worked in the Antarctic since the 1990s. The data are publicly available through biodiversity.aq and the Ocean Biogeographic Information System. The archive includes tracking data from over 70 contributors across 12 national Antarctic programs, and includes data from 17 predator species, 4060 individual animals, and over 2.9 million observed locations.

Finding mesopelagic prey in a changing Southern Ocean.

Mesopelagic fish and squid occupy ocean depths extending below the photic zone and their vertical migrations represent a massive pathway moving energy and carbon through the water column. Their spatio-temporal distribution is however, difficult to map across remote regions particularly the vast Southern Ocean. This represents a key gap in understanding biogeochemical processes, marine ecosystem structure, and how changing ocean conditions will affect marine predators, which depend upon mesopelagic prey. We infer mesopelagic prey vertical distribution and relative abundance in the Indian sector of the Southern Ocean (20° to 130°E) with a novel approach using predator-derived indices. Fourteen years of southern elephant seal tracking and dive data, from the open ocean between the Antarctic Polar Front and the southern Antarctic Circumpolar Current front, clearly show that the vertical distribution of mesopelagic prey is influenced by the physical hydrographic processes that structure their habitat. Mesopelagic prey have a more restricted vertical migration and higher relative abundance closer to the surface where Circumpolar Deep Water rises to shallower depths. Combining these observations with a future projection of Southern Ocean conditions we show that changes in the coupling of surface and deep waters will potentially redistribute mesopelagic prey. These changes are small overall, but show important spatial variability: prey will increase in relative abundance to the east of the Kerguelen Plateau but decrease to the west. The consequences for deep-diving specialists such as elephant seals and whales over this time scale will likely be minor, but the changes in mesoscale vertical energy flow have implications for predators that forage within the mesopelagic zone as well as the broader pelagic ecosystem.

Coastal polynyas: Winter oases for subadult southern elephant seals in East Antarctica.

Antarctic coastal polynyas are regions of persistent open water and are thought to be key bio-physical features within the sea-ice zone. However, their use by the upper trophic levels of ecosystems remains unclear. A unique bio-physical dataset recorded by southern elephant seals reveals that East Antarctic polynyas are a key winter foraging habitat for male seals. During their post-moult trips from Isles Kerguelen to the Antarctic continental shelf, a total of 18 out of 23 seals visited 9 different polynyas, spending on average 25 ± 20% (up to 75%) of their total trip time inside polynyas. Changes in seal foraging and diving behaviours are observed inside polynyas as compared to outside polynyas. Two polynya usages by seals are observed for the inactive and active polynya phases, pointing to different seasonal peaks in prey abundance. During the active polynya phase, we link seal foraging behaviour to changes in the physical stability of the water-column, which likely impact the seasonal biological dynamics within polynyas.

Variability in sea ice cover and climate elicit sex specific responses in an Antarctic predator.

Contrasting regional changes in Southern Ocean sea ice have occurred over the last 30 years with distinct regional effects on ecosystem structure and function. Quantifying how Antarctic predators respond to such changes provides the context for predicting how climate variability/change will affect these assemblages into the future. Over an 11-year time-series, we examine how inter-annual variability in sea ice concentration and advance affect the foraging behaviour of a top Antarctic predator, the southern elephant seal. Females foraged longer in pack ice in years with greatest sea ice concentration and earliest sea ice advance, while males foraged longer in polynyas in years of lowest sea ice concentration. There was a positive relationship between near-surface meridional wind anomalies and female foraging effort, but not for males. This study reveals the complexities of foraging responses to climate forcing by a poleward migratory predator through varying sea ice property and dynamic anomalies.

Contrasting behavior between two populations of an ice-obligate predator in East Antarctica.

The Austral autumn-winter is a critical period for capital breeders such as Weddell seals that must optimize resource acquisition and storage to provision breeding in the subsequent spring. However, how Weddell seals find food in the winter months remains poorly documented. We equipped adult Weddell seals after their annual molt with satellite-relayed data loggers at two sites in East Antarctica: Dumont D'Urville (n = 12, DDU) and Davis (n = 20). We used binomial generalized mixed-effect models to investigate Weddell seals' behavioral response (i.e., "hunting" vs. "transit") to physical aspects of their environment (e.g., ice concentration). Weddell seal foraging was concentrated to within 5 km of a breathing hole, and they appear to move between holes as local food is depleted. There were regional differences in behavior so that seals at Davis traveled greater distances (three times more) and spent less time in hunting mode (half the time) than seals at DDU. Despite these differences, hunting dives at both locations were pelagic, concentrated in areas of high ice concentration, and over areas of complex bathymetry. There was also a seasonal change in diving behavior from transiting early in the season to more hunting during winter. Our observations suggest that Weddell seal foraging behavior is plastic and that they respond behaviorally to changes in their environment to maximize food acquisition and storage. Such plasticity is a hallmark of animals that live in very dynamic environments such as the high Antarctic where resources are unpredictable.

Influence of environmental parameters on movements and habitat utilization of humpback whales (Megaptera novaeangliae) in the Madagascar breeding ground.

Assessing the movement patterns and key habitat features of breeding humpback whales is a prerequisite for the conservation management of this philopatric species. To investigate the interactions between humpback whale movements and environmental conditions off Madagascar, we deployed 25 satellite tags in the northeast and southwest coast of Madagascar. For each recorded position, we collated estimates of environmental variables and computed two behavioural metrics: behavioural state of 'transiting' (consistent/directional) versus 'localized' (variable/non-directional), and active swimming speed (i.e. speed relative to the current). On coastal habitats (i.e. bathymetry < 200 m and in adjacent areas), females showed localized behaviour in deep waters (191 ± 20 m) and at large distances (14 ± 0.6 km) from shore, suggesting that their breeding habitat extends beyond the shallowest waters available close to the coastline. Males' active swimming speed decreased in shallow waters, but environmental parameters did not influence their likelihood to exhibit localized movements, which was probably dominated by social factors instead. In oceanic habitats, both males and females showed localized behaviours in shallow waters and favoured high chlorophyll-a concentrations. Active swimming speed accounts for a large proportion of observed movement speed; however, breeding humpback whales probably exploit prevailing ocean currents to maximize displacement. This study provides evidence that coastal areas, generally subject to strong human pressure, remain the core habitat of humpback whales off Madagascar. Our results expand the knowledge of humpback whale habitat use in oceanic habitat and response to variability of environmental factors such as oceanic current and chlorophyll level.

A new method to quantify within dive foraging behaviour in marine predators.

Studies on diving behaviour classically divide a dive into three phases: the descent, bottom and ascent phases, with foraging assumed to occur during the bottom phase. The greater complexity of dive revealed through modern, high resolution data highlights the need to re-assess this approach and to consider a larger number of phases within individual dives. Two southern elephant seals (SES) were fitted with a head mounted Time Depth Recorder (TDR) and an accelerometer from which prey capture attempts were estimated. A Weddell seal was also fitted with a TDR. TDRs for both species recorded depth once per second. We quantified the within dive behaviour using an automated broken stick algorithm identifying the optimal number of segments within each dive. The vertical sinuosity of the segments was used to infer two types of behaviours, with highly sinuous segments indicating "hunting" and less sinuous segments indicating "transiting". Using the broken stick method the seals alternated between "hunting" and "transit" modes with an average of 6±2 and 7±0.02 behavioural phases within each dive for the Weddell seal and SES, respectively. In SES, 77% of prey capture attempts (identified from the acceleration data) occurred in highly sinuous phases ("hunting") as defined by our new approach. SES spent more time in transit mode within a dive, and hunting mostly occurred during the bottom phase. Conversely the Weddell seal spent more time in hunting mode which also occurred during bottom phase but occurred mostly at shallower depths. Such differences probably reflect different foraging tactics and habitat use. For both species, hunting time differs significantly from bottom time previously used as a proxy for the time spent foraging in a dive. The hunting time defined by our method therefore provides a more accurate fine-scale description of the seals' foraging behaviour.

A Southern Indian Ocean database of hydrographic profiles obtained with instrumented elephant seals.

The instrumentation of southern elephant seals with satellite-linked CTD tags has offered unique temporal and spatial coverage of the Southern Indian Ocean since 2004. This includes extensive data from the Antarctic continental slope and shelf regions during the winter months, which is outside the conventional areas of Argo autonomous floats and ship-based studies. This landmark dataset of around 75,000 temperature and salinity profiles from 20-140 °E, concentrated on the sector between the Kerguelen Islands and Prydz Bay, continues to grow through the coordinated efforts of French and Australian marine research teams. The seal data are quality controlled and calibrated using delayed-mode techniques involving comparisons with other existing profiles as well as cross-comparisons similar to established protocols within the Argo community, with a resulting accuracy of ±0.03 °C in temperature and ±0.05 in salinity or better. The data offer invaluable new insights into the water masses, oceanographic processes and provides a vital tool for oceanographers seeking to advance our understanding of this key component of the global ocean climate.

Integrative modelling of animal movement: incorporating in situ habitat and behavioural information for a migratory marine predator.

A fundamental goal in animal ecology is to quantify how environmental (and other) factors influence individual movement, as this is key to understanding responsiveness of populations to future change. However, quantitative interpretation of individual-based telemetry data is hampered by the complexity of, and error within, these multi-dimensional data. Here, we present an integrative hierarchical Bayesian state-space modelling approach where, for the first time, the mechanistic process model for the movement state of animals directly incorporates both environmental and other behavioural information, and observation and process model parameters are estimated within a single model. When applied to a migratory marine predator, the southern elephant seal (Mirounga leonina), we find the switch from directed to resident movement state was associated with colder water temperatures, relatively short dive bottom time and rapid descent rates. The approach presented here can have widespread utility for quantifying movement-behaviour (diving or other)-environment relationships across species and systems.

Assessment of scale-dependent foraging behaviour in southern elephant seals incorporating the vertical dimension: a development of the First Passage Time method.

1. Identifying the spatial scales at which top marine predators forage is important for understanding oceanic ecosystems. Several methods quantify how individuals concentrate their search effort along a given path. Among these, First-Passage Time (FPT) analysis is particularly useful to identify transitions in movement patterns (e.g. between searching and feeding). This method has mainly been applied to terrestrial animals or flying seabirds that have little or no vertical component to their foraging, so we examined the differences between classic FPT and a modification of this approach using the time spent at the bottom of a dive for characterizing the foraging activity of a diving predator: the southern elephant seal. 2. Satellite relayed data loggers were deployed on 20 individuals during three successive summers at the Kerguelen Islands, providing a total of 72 978 dives from eight juvenile males and nine adult females. 3. Spatial scales identified using the time spent at the bottom of a dive ( = 68.2 +/- 42.1 km) were smaller than those obtained by the classic FPT analysis ( = 104.7 +/- 67.3 km). Moreover, foraging areas identified using the new approach clearly overlapped areas where individuals increased their body condition, indicating that it accurately reflected the foraging activity of the seals. 4. These results suggest that incorporating the vertical dimension into FPT provides a different result to the surface path alone. Close to the Antarctic continent, within the pack-ice, sinuosity of the path could be explained by a high sea-ice concentration (restricting elephant seal movements), and was not necessarily related to foraging activity. 5. Our approach distinguished between actual foraging activity and changes in behaviour induced by the physical environment like sea ice, and could be applied to other diving predators. Inclusion of diving parameters appears to be essential to identify the spatial scale of foraging areas of diving animals.

Successful foraging zones of southern elephant seals from the Kerguelen Islands in relation to oceanographic conditions.

Southern elephant seals, Mirounga leonina, undertake large-scale oceanic movements to access favourable foraging areas. Successful foraging areas of elephant seals from the Kerguelen Islands are investigated here in relation to oceanographic parameters. Movements and diving activity of the seals as well as oceanographic data were collected through a new generation of satellite relayed devices measuring and transmitting locations, pressure, temperature and salinity. For the first time, we have associated foraging behaviour, determined by high increased sinuosity in tracks, and dive density (i.e. number of dives performed per kilometre covered), and changes in body condition, determined by variations in drift rate obtained from drift dives, to identify the oceanographic conditions of successful foraging zones for this species. Two main sectors, one close to the Antarctic continent and the other along the Polar Front (PF), where both foraging activity and body condition increase, seem to be of particular interest for the seals. Within these regions, some seals tended to focus their foraging activity on zones with particular temperature signatures. Along the Antarctic continent, some seals targeted colder waters on the sea bottom during benthic dives, while at the PF the favourable zones tended to be warmer. The possible negative effect of colder waters in Antarctic on the swimming performances of potential fish or squid prey could explain the behaviour of elephant seals in these zones, while warmer waters within the PF could correspond to the optimal conditions for potential myctophid prey of elephant seals.

Why do macaroni penguins choose shallow body angles that result in longer descent and ascent durations?

It is generally assumed that air-breathing aquatic animals always choose the shortest route to minimize duration for transit between the surface and foraging depth in order to maximize the proportion of time spent foraging. However, empirical data indicate that the body angles of some diving animals are rarely vertical during descent and ascent. Why do they choose shallower body angles that result in longer descent and ascent durations? To investigate this question, we attached acceleration data loggers to eight female macaroni penguins, breeding on the Kerguelen Islands (48 degrees 45'-50 degrees 00' S, 68 degrees 45'-70 degrees 58' E; South Indian Ocean), to record depth, two-dimensional acceleration (stroke cycle frequency and body angle) and temperature. We investigated how they controlled body angle and allocated their submerged time. The instrumented females performed multiple dives (N=6952) with a mean dive depth for each bird ranging from 24.5+/-28.5 m to 56.4+/-75.1 m. Mean body angles during descent and ascent were not vertical. There was large variation in mean descent and ascent angles for a given dive depth, which, in turn, caused large variation in descent and ascent duration. Body angles were significantly correlated with time spent at the bottom-phase of the dive. Birds that spent long periods at the bottom exhibited steep body angles during ascent and subsequent descent. By contrast, they adopted shallow body angles after they had short or no bottom phases. Our results suggest that macaroni penguins stay at the bottom longer after encountering a good prey patch and then travel to the surface at steep body angles. If they do not encounter prey, they discontinue the dive, without staying at the bottom, ascend at shallow body angles and descend at shallow body angles in a subsequent dive. A shallow body angle can increase the horizontal distance covered during a dive, contributing to the move into a more profitable area in the following dive. During the ascent, in particular, macaroni penguins stopped beating their flippers. The buoyantly gliding penguins can move horizontally with minimum stroking effort before reaching the surface.