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.

Long-term stability in the circumpolar foraging range of a Southern Ocean predator between the eras of whaling and rapid climate change.

Assessing environmental changes in Southern Ocean ecosystems is difficult due to its remoteness and data sparsity. Monitoring marine predators that respond rapidly to environmental variation may enable us to track anthropogenic effects on ecosystems. Yet, many long-term datasets of marine predators are incomplete because they are spatially constrained and/or track ecosystems already modified by industrial fishing and whaling in the latter half of the 20th century. Here, we assess the contemporary offshore distribution of a wide-ranging marine predator, the southern right whale (SRW, Eubalaena australis), that forages on copepods and krill from ~30°S to the Antarctic ice edge (>60°S). We analyzed carbon and nitrogen isotope values of 1,002 skin samples from six genetically distinct SRW populations using a customized assignment approach that accounts for temporal and spatial variation in the Southern Ocean phytoplankton isoscape. Over the past three decades, SRWs increased their use of mid-latitude foraging grounds in the south Atlantic and southwest (SW) Indian oceans in the late austral summer and autumn and slightly increased their use of high-latitude (>60°S) foraging grounds in the SW Pacific, coincident with observed changes in prey distribution and abundance on a circumpolar scale. Comparing foraging assignments with whaling records since the 18th century showed remarkable stability in use of mid-latitude foraging areas. We attribute this consistency across four centuries to the physical stability of ocean fronts and resulting productivity in mid-latitude ecosystems of the Southern Ocean compared with polar regions that may be more influenced by recent climate change.

A novel method for identifying fine-scale bottom-use in a benthic-foraging pinniped.

BACKGROUND: For diving, marine predators, accelerometer and magnetometer data provides critical information on sub-surface foraging behaviours that cannot be identified from location or time-depth data. By measuring head movement and body orientation, accelerometers and magnetometers can help identify broad shifts in foraging movements, fine-scale habitat use and energy expenditure of terrestrial and marine species. Here, we use accelerometer and magnetometer data from tagged Australian sea lions and provide a new method to identify key benthic foraging areas. As Australian sea lions are listed as endangered by the IUCN and Australian legislation, identifying key areas for the species is vital to support targeted management of populations. METHODS: Firstly, tri-axial magnetometer and accelerometer data from adult female Australian sea lions is used in conjunction with GPS and dive data to dead-reckon their three-dimensional foraging paths. We then isolate all benthic phases from their foraging trips and calculate a range of dive metrics to characterise their bottom usage. Finally, k-means cluster analysis is used to identify core benthic areas utilised by sea lions. Backwards stepwise regressions are then iteratively performed to identify the most parsimonious model for describing bottom usage and its included predictor variables. RESULTS: Our results show distinct spatial partitioning in benthic habitat-use by Australian sea lions. This method has also identified individual differences in benthic habitat-use. Here, the application of high-resolution magnetometer/accelerometer data has helped reveal the tortuous foraging movements Australian sea lions use to exploit key benthic marine habitats and features. CONCLUSIONS: This study has illustrated how magnetometer and accelerometer data can provide a fine-scale description of the underwater movement of diving species, beyond GPS and depth data alone, For endangered species like Australian sea lions, management of populations must be spatially targeted. Here, this method demonstrates a fine-scale analysis of benthic habitat-use which can help identify key areas for both marine and terrestrial species. Future integration of this method with concurrent habitat and prey data would further augment its power as a tool for understanding the foraging behaviours of species.

Fur seals do, but sea lions don't - cross taxa insights into exhalation during ascent from dives.

Management of gases during diving is not well understood across marine mammal species. Prior to diving, phocid (true) seals generally exhale, a behaviour thought to assist with the prevention of decompression sickness. Otariid seals (fur seals and sea lions) have a greater reliance on their lung oxygen stores, and inhale prior to diving. One otariid, the Antarctic fur seal (Arctocephalus gazella), then exhales during the final 50-85% of the return to the surface, which may prevent another gas management issue: shallow-water blackout. Here, we compare data collected from animal-attached tags (video cameras, hydrophones and conductivity sensors) deployed on a suite of otariid seal species to examine the ubiquity of ascent exhalations for this group. We find evidence for ascent exhalations across four fur seal species, but that such exhalations are absent for three sea lion species. Fur seals and sea lions are no longer genetically separated into distinct subfamilies, but are morphologically distinguished by the thick underfur layer of fur seals. Together with their smaller size and energetic dives, we suggest their air-filled fur might underlie the need to perform these exhalations, although whether to reduce buoyancy and ascent speed, for the avoidance of shallow-water blackout or to prevent other cardiovascular management issues in their diving remains unclear. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Two behavioural traits promote fine-scale species segregation and moderate hybridisation in a recovering sympatric fur seal population.

BACKGROUND: In systems where two or more species experience secondary contact, behavioural factors that regulate interspecific gene flow may be important for maintaining species boundaries and reducing the incidence of hybridisation. At subantarctic Macquarie Island, two species of fur seal breed in close proximity to one another, hybridise at very high levels (up to 21% of hybrid pups are born annually), yet retain discrete gene pools. Using spatial and genetic information collected for pups and adults over twelve years, we assessed two behavioural traits - inter-annual site fidelity and differences in habitat use between the species - as possible contributors to the maintenance of this species segregation. Further, we explored the breakdown of these traits in pure-species individuals and hybrids. RESULTS: We found virtually complete spatial segregation of the parental species, with only one exception; a single territory that contained adults of both species and also the highest concentration of hybrid pups. The spatial distribution of each species was closely linked to habitat type (pebbled vs boulder beaches), with members of each species breeding almost exclusively on one type or the other but hybrids breeding on both or at the junction between habitats. Inter-annual site fidelity was high for both sexes of pure-species adults, with 66% of females and all males returning to the same territory or a neighbouring one in different years. An important consequence for pure females of breeding on the 'wrong' habitat type, and thus in a heterospecific aggregation, was the production of hybrid pups. Low habitat fidelity of hybrid females facilitated bi-directional backcrossing, resulting in more diverse hybrid offspring. CONCLUSION: In a disturbed system where two sympatric fur seal species breed in close proximity, discrete gene pools are retained by extremely fine-scale and strong spatial segregation of the species. Two behavioural traits were found to be important in maintaining this stable population structure, and habitat type was a strong indicator of where species locate and a potentially powerful predictor of future directions of hybridisation. A direct consequence of the breakdown of this trait was the production of hybrid offspring, which may have severe implications if hybrids have reduced fitness.

Publisher Correction: The genetic legacy of extreme exploitation in a polar vertebrate.

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

Satellite derived offshore migratory movements of southern right whales (Eubalaena australis) from Australian and New Zealand wintering grounds.

Southern right whales (Eubalaena australis) migrate between Austral-winter calving and socialising grounds to offshore mid- to high latitude Austral-summer feeding grounds. In Australasia, winter calving grounds used by southern right whales extend from Western Australia across southern Australia to the New Zealand sub-Antarctic Islands. During the Austral-summer these whales are thought to migrate away from coastal waters to feed, but the location of these feeding grounds is only inferred from historical whaling data. We present new information on the satellite derived offshore migratory movements of six southern right whales from Australasian wintering grounds. Two whales were tagged at the Auckland Islands, New Zealand, and the remaining four at Australian wintering grounds, one at Pirates Bay, Tasmania, and three at Head of Bight, South Australia. The six whales were tracked for an average of 78.5 days (range: 29 to 150) with average individual distance of 38 km per day (range: 20 to 61 km). The length of individually derived tracks ranged from 645-6,381 km. Three likely foraging grounds were identified: south-west Western Australia, the Subtropical Front, and Antarctic waters, with the Subtropical Front appearing to be a feeding ground for both New Zealand and Australian southern right whales. In contrast, the individual tagged in Tasmania, from a sub-population that is not showing evidence of post-whaling recovery, displayed a distinct movement pattern to much higher latitude waters, potentially reflecting a different foraging strategy. Variable population growth rates between wintering grounds in Australasia could reflect fidelity to different quality feeding grounds. Unlike some species of baleen whale populations that show movement along migratory corridors, the new satellite tracking data presented here indicate variability in the migratory pathways taken by southern right whales from Australia and New Zealand, as well as differences in potential Austral summer foraging grounds.

The genetic legacy of extreme exploitation in a polar vertebrate.

Understanding the effects of human exploitation on the genetic composition of wild populations is important for predicting species persistence and adaptive potential. We therefore investigated the genetic legacy of large-scale commercial harvesting by reconstructing, on a global scale, the recent demographic history of the Antarctic fur seal (Arctocephalus gazella), a species that was hunted to the brink of extinction by 18th and 19th century sealers. Molecular genetic data from over 2,000 individuals sampled from all eight major breeding locations across the species' circumpolar geographic distribution, show that at least four relict populations around Antarctica survived commercial hunting. Coalescent simulations suggest that all of these populations experienced severe bottlenecks down to effective population sizes of around 150-200. Nevertheless, comparably high levels of neutral genetic variability were retained as these declines are unlikely to have been strong enough to deplete allelic richness by more than around 15%. These findings suggest that even dramatic short-term declines need not necessarily result in major losses of diversity, and explain the apparent contradiction between the high genetic diversity of this species and its extreme exploitation history.

Correction: Satellite derived offshore migratory movements of southern right whales (Eubalaena australis) from Australian and New Zealand wintering grounds.

[This corrects the article DOI: 10.1371/journal.pone.0231577.].

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.

RAD Sequencing and a Hybrid Antarctic Fur Seal Genome Assembly Reveal Rapidly Decaying Linkage Disequilibrium, Global Population Structure and Evidence for Inbreeding.

Recent advances in high throughput sequencing have transformed the study of wild organisms by facilitating the generation of high quality genome assemblies and dense genetic marker datasets. These resources have the potential to significantly advance our understanding of diverse phenomena at the level of species, populations and individuals, ranging from patterns of synteny through rates of linkage disequilibrium (LD) decay and population structure to individual inbreeding. Consequently, we used PacBio sequencing to refine an existing Antarctic fur seal (Arctocephalus gazella) genome assembly and genotyped 83 individuals from six populations using restriction site associated DNA (RAD) sequencing. The resulting hybrid genome comprised 6,169 scaffolds with an N50 of 6.21 Mb and provided clear evidence for the conservation of large chromosomal segments between the fur seal and dog (Canis lupus familiaris). Focusing on the most extensively sampled population of South Georgia, we found that LD decayed rapidly, reaching the background level by around 400 kb, consistent with other vertebrates but at odds with the notion that fur seals experienced a strong historical bottleneck. We also found evidence for population structuring, with four main Antarctic island groups being resolved. Finally, appreciable variance in individual inbreeding could be detected, reflecting the strong polygyny and site fidelity of the species. Overall, our study contributes important resources for future genomic studies of fur seals and other pinnipeds while also providing a clear example of how high throughput sequencing can generate diverse biological insights at multiple levels of organization.

Entanglement of Australian sea lions and New Zealand fur seals in lost fishing gear and other marine debris before and after Government and industry attempts to reduce the problem.

In recent years, Australian governments and fishing industry associations have developed guiding principles aimed at reducing the impact of fishing on non-target species and the benthos and increasing community awareness of their efforts. To determine whether they reduced seal entanglement in lost fishing gear and other marine debris, we analysed Australian sea lion and New Zealand fur seal entanglement data collected from Kangaroo Island, South Australia. Contrary to our expectations, we found that entanglement rates did not decrease in recent years. The Australian sea lion entanglement rate (1.3% in 2002) and the New Zealand fur seal entanglement rate (0.9% in 2002) are the third and fourth highest reported for any seal species. Australian sea lions were most frequently entangled in monofilament gillnet that most likely originated from the shark fishery, which operates in the region where sea lions forage--south and east of Kangaroo Island. In contrast, New Zealand fur seals were most commonly entangled in loops of packing tape and trawl net fragments suspected to be from regional rock lobster and trawl fisheries. Based on recent entanglement studies, we estimate that 1478 seals die from entanglement each year in Australia. We discuss remedies such as education programs and government incentives that may reduce entanglements.

Steady as he goes: at-sea movement of adult male Australian sea lions in a dynamic marine environment.

The southern coastline of Australia forms part of the worlds' only northern boundary current system. The Bonney Upwelling occurs every austral summer along the south-eastern South Australian coastline, a region that hosts over 80% of the worlds population of an endangered endemic otariid, the Australian sea lion. We present the first data on the movement characteristics and foraging behaviour of adult male Australian sea lions across their South Australian range. Synthesizing telemetric, oceanographic and isotopic datasets collected from seven individuals enabled us to characterise individual foraging behaviour over an approximate two year time period. Data suggested seasonal variability in stable carbon and nitrogen isotopes that could not be otherwise explained by changes in animal movement patterns. Similarly, animals did not change their foraging patterns despite fine-scale spatial and temporal variability of the upwelling event. Individual males tended to return to the same colony at which they were tagged and utilized the same at-sea regions for foraging irrespective of oceanographic conditions or time of year. Our study contrasts current general assumptions that male otariid life history strategies should result in greater dispersal, with adult male Australian sea lions displaying central place foraging behaviour similar to males of other otariid species in the region.

Effects of an electric field on white sharks: in situ testing of an electric deterrent.

Elasmobranchs can detect minute electromagnetic fields, <1 nV cm(-1), using their ampullae of Lorenzini. Behavioural responses to electric fields have been investigated in various species, sometimes with the aim to develop shark deterrents to improve human safety. The present study tested the effects of the Shark Shield Freedom7™ electric deterrent on (1) the behaviour of 18 white sharks (Carcharodon carcharias) near a static bait, and (2) the rates of attacks on a towed seal decoy. In the first experiment, 116 trials using a static bait were performed at the Neptune Islands, South Australia. The proportion of baits taken during static bait trials was not affected by the electric field. The electric field, however, increased the time it took them to consume the bait, the number of interactions per approach, and decreased the proportion of interactions within two metres of the field source. The effect of the electric field was not uniform across all sharks. In the second experiment, 189 tows using a seal decoy were conducted near Seal Island, South Africa. No breaches and only two surface interactions were observed during the tows when the electric field was activated, compared with 16 breaches and 27 surface interactions without the electric field. The present study suggests that the behavioural response of white sharks and the level of risk reduction resulting from the electric field is contextually specific, and depends on the motivational state of sharks.

Assessing morphological and DNA-based diet analysis techniques in a generalist predator, the arrow squid Nototodarus gouldi.

Establishing the diets of marine generalist consumers is difficult, with most studies limited to the use of morphological methods for prey identification. Such analyses rely on the preservation of diagnostic hard parts, which can limit taxonomic resolution and introduce biases. DNA-based analyses provide a method to assess the diets of marine species, potentially overcoming many of the limitations introduced by other techniques. This study compared the effectiveness of morphological and DNA-based analysis for determining the diet of a free-ranging generalist predator, the arrow squid (Nototodarus gouldi). A combined approach was more effective than using either of the methods in isolation. Nineteen unique prey taxa were identified, of which six were found by both methods, 10 were only detected using DNA and three were only identified using morphological methods. Morphological techniques only found 50% of the total number of identifiable prey taxa, whereas DNA-based techniques found 84%. This study highlights the benefits of using a combination of techniques to detect and identify prey of generalist marine consumers.

Multiple mating strategies explain unexpected genetic mixing of New Zealand fur seals with two congenerics in a recently recolonized population.

Human impacts on natural systems can cause local population extinctions, which may promote redistribution of taxa and secondary contact between divergent lineages. In mammalian populations that have mating systems shaped by polygyny and sexual selection, the potential for hybridization to ensue and persist depends on individual and demographic factors. At Macquarie Island, a recently formed fur seal population is comprised of both sexes of breeding Antarctic (Arctocephalus gazella) and subantarctic (A. tropicalis) fur seals, and an itinerant collection of male New Zealand fur seals (A. forsteri), presumed to be non-breeders due to their absence from principle breeding areas. The mating system of the three species is described as resource-defence polygyny: males defend beach territories containing breeding females for exclusive mating rights. A recent genetic study identified a high level of hybridization in the population (17-30%), unexpectedly involving all three species. This study examined the source of involvement in breeding by A. forsteri with respect to mating strategies operating in the population. Ninety-five (10%) pups born from 1992 to 2003 were genetically identified as New Zealand hybrids. Most resulted from reproduction within territories by New Zealand hybrids of both sexes, although some were conceived extra-territorially, indicating that males successfully utilize strategies other than territory holding to achieve paternities. Female reproductive status influenced mating partner and mating location, and females without pups were more likely to conceive extra-territorially and with A. forsteri males. This study illustrates an important consequence of low heterospecific discrimination in a sympatric population of long-lived mammals.

Lower reproductive success in hybrid fur seal males indicates fitness costs to hybridization.

Hybridization among organisms can potentially contribute to the processes of evolution, but this depends on the fitness of hybrids relative to parental species. A small, recently formed population of fur seals on subantarctic Macquarie Island contains a high proportion of hybrids (17-30%) derived from combinations of three parental species: Antarctic, subantarctic and New Zealand fur seals. Mitochondrial control-region data (restriction fragment length polymorphisms) and nine microsatellites were used to determine the species composition of breeding adults, and hybrid male fitness was measured by comparing reproductive success (number of genetically inferred paternities) of hybrid and pure-species territory males over 6 years. No correlations were found between male reproductive success and three genetic measures of outbreeding, but this may be due to a relatively small number of dominant males analysed. Territory males fathered 63% of pups, but hybrid males had lower reproductive success than pure-species males despite having the same ability to hold territories. A greater proportion of females in hybrid male territories conceived extra-territorially than those in territories of pure-species males, and most (70 of 82) mated with conspecifics. This suggests the presence of reproductive isolating mechanisms that promote positive assortative mating and reduce the production of hybrid offspring. Although we found no evidence for male sterility in the population, mechanisms that reduce lifetime reproductive success may act to decrease the frequency of hybrids. Our study has identified a disadvantage of hybridization - reduced reproductive success of hybrid sons - that may be contributing to the persistence of pure lineages at Macquarie Island and the temporal decline in hybridization observed there.

Drinking behaviour and water turnover rates of Antarctic fur seal pups: implications for the estimation of milk intake by isotopic dilution.

The estimation of milk consumption in free-ranging seals using tritium dilution techniques makes the key assumption that the animals drink no pre-formed water during the experimental period. However, frequent observations of unweaned Antarctic fur seal pups drinking water at Iles Kerguelen necessitated the testing of this assumption. We estimated water flux rates of 30 pups (10.7+/-0.3 kg) in four experimental groups by isotopic dilution over 4 days. The groups were: (1) pups held in an open air enclosure without access to water to estimate fasting metabolic water production (MWP); (2) free-ranging pups not administered additional water; (3) pups held in an open air enclosure and given a total of 300 ml of fresh water to verify technique accuracy; and (4) free-ranging pups given 200 ml of fresh water. Pups without access to water exhibited water flux rates (20.5+/-0.8 ml kg(-1)d(-1)), which were significantly lower than those observed for the free-ranging group (33.0+/-1.7 ml kg(-1) d(-1)). Mean estimated pre-formed water intake for the free-ranging experimental groups was 12.6 ml kg(-1) d(-1). Thus, MWP, measured as total water intake during fasting, may be significantly over-estimated in free-ranging Antarctic fur seal pups at Iles Kerguelen and at other sites and subsequently milk intake rates may be underestimated.