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.

Environmental correlates of temporal variation in the prey species of Australian fur seals inferred from scat analysis.

Marine ecosystems in southeastern Australia are responding rapidly to climate change. We monitored the diet of the Australian fur seal (Arctocephalus pusillus doriferus), a key marine predator, over 17 years (1998-2014) to examine temporal changes. Frequency of occurrence (FO) of prey was used as a proxy for ecosystem change. Hard part analysis identified 71 prey taxa, with eight dominant taxa in greater than 70% of samples and predominantly included benthic and small pelagic fish. FO changed over time, e.g. redbait (Emmelichthys nitidus) reduced after 2005 when jack mackerel (Trachurus declivis) increased, and pilchard (Sardinops sajax) increased after 2009. Using generalized additive models, correlations between FO and environmental variables were evident at both the local (e.g. wind, sea surface temperature (SST)) and regional (e.g. El Niño-Southern Oscillation Index (SOI), Southern Annular Mode (SAM)) scales, with redbait and pilchard showing the best model fits (greater than 75% deviance explained). Positive SAM was correlated to FO for both species, and wind and season were important for redbait, while SOI and SST were important for pilchard. Both large-scale and regional processes influenced prey taxa in variable ways. We predict that the diverse and adaptable diet of the Australian fur seal will be advantageous in a rapidly changing ecosystem.

Sustained reduction in numbers of Australian fur seal pups: Implications for future population monitoring.

Fur seal populations in the Southern Hemisphere were plundered in the late 1700s and early 1800s to provide fur for a clothing industry. Millions of seals were killed resulting in potentially major ecosystem changes across the Southern Hemisphere, the consequences of which are unknown today. Following more than a century of population suppression, partly through on-going harvesting, many of the fur seal populations started to recover in the late 1900s. Australian fur seals (Arctocephalus pusillus doriferus), one of the most geographically constrained fur seal species, followed this trend. From the 1940s to 1986, pup production remained at approximately 10,000 per year, then significant growth commenced. By 2007, live pup abundance had recovered to approximately 21,400 per year and recovery was expected to continue However, a species-wide survey in 2013 recorded a 20% decline, to approximately 16,500 live pups. It was not known if this decline was due to 2013 being a poor breeding year or a true population reduction. Here we report the results of a population-wide survey conducted in 2017 and annual monitoring at the most productive colony, Seal Rocks, Victoria that recorded a large decline in live pup abundance (-28%). Sustained lower pup numbers at Seal Rocks from annual counts between 2012-2017 (mean = 2908 ± 372 SD), as well as the population-wide estimate of 16,903 live pups in 2017, suggest that the pup numbers for the total population have remained at the lower level observed in 2013 and that the 5-yearly census results are not anomalies or representative of poor breeding seasons. Potential reasons for the decline, which did not occur range-wide but predominantly in the most populated and long-standing breeding sites, are discussed. To enhance adaptive management of this species, methods for future monitoring of the population are also presented. Australian fur seals occupy several distinct regions influenced by different currents and upwellings: range-wide pup abundance monitoring enables comparisons of ecosystem status across these regions. Forces driving change in Australian fur seal pup numbers are likely to play across other marine ecosystems, particularly in the Southern Hemisphere where most fur seals live.

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.

Analysis of Australian fur seal diet by pyrosequencing prey DNA in faeces.

DNA-based techniques have proven useful for defining trophic links in a variety of ecosystems and recently developed sequencing technologies provide new opportunities for dietary studies. We investigated the diet of Australian fur seals (Arctocephalus pusillus doriferus) by pyrosequencing prey DNA from faeces collected at three breeding colonies across the seals' range. DNA from 270 faecal samples was amplified with four polymerase chain reaction primer sets and a blocking primer was used to limit amplification of fur seal DNA. Pooled amplicons from each colony were sequenced using the Roche GS-FLX platform, generating > 20,000 sequences. Software was developed to sort and group similar sequences. A total of 54 bony fish, 4 cartilaginous fish and 4 cephalopods were identified based on the most taxonomically informative amplicons sequenced (mitochondrial 16S). The prevalence of sequences from redbait (Emmelichthys nitidus) and jack mackerel (Trachurus declivis) confirm the importance of these species in the seals' diet. A third fish species, blue mackerel (Scomber australasicus), may be a more important prey species than previously recognised. There were major differences in the proportions of prey DNA recovered in faeces from different colonies, probably reflecting differences in prey availability. Parallel hard-part analysis identified largely the same main prey species as did the DNA-based technique, but with lower species diversity and no remains from cartilaginous prey. The pyrosequencing approach presented significantly expands the capabilities of DNA-based methods of dietary analysis and is suitable for large-scale diet investigations on a broad range of animals.

Impact of rising sea levels on Australian fur seals.

Global warming is leading to many unprecedented changes in the ocean-climate system. Sea levels are rising at an increasing rate and are amplifying the impact of storm surges along coastlines. As variability in the timing and strength of storm surges has been shown to affect pup mortality in the Australian fur seal (Arctocephalus pusillus doriferus), there is a need to identify the potential impacts of increased sea level and storm surges on the breeding areas of this important marine predator in Bass Strait, south-eastern Australia. Using high-resolution aerial photography and topographic data, the present study assessed the impacts of future inundation levels on both current and potential breeding habitats at each colony. Inundation from storm surges, based on a predicted rise in sea level, was modeled at each colony from 2012 to 2100. As sea level increases, progressively less severe storm surge conditions will be required to exceed current inundation levels and, thus, have the potential for greater impacts on pup mortality at Australian fur seal colonies. The results of the present study indicate that by 2100, a 1-in-10 year storm will inundate more habitat on average than a present-day 1-in-100 year storm. The study highlights the site-specific nature of storm surge impacts, and in particular the importance of local colony topography and surrounding bathymetry with small, low-lying colonies impacted the most. An increased severity of storm surges will result in either an increase in pup mortality rates associated with storm surges, or the dispersal of individuals to higher ground and/or new colonies.

Understanding meta-population trends of the Australian fur seal, with insights for adaptive monitoring.

Effective ecosystem-based management requires estimates of abundance and population trends of species of interest. Trend analyses are often limited due to sparse or short-term abundance estimates for populations that can be logistically difficult to monitor over time. Therefore it is critical to assess regularly the quality of the metrics in long-term monitoring programs. For a monitoring program to provide meaningful data and remain relevant, it needs to incorporate technological improvements and the changing requirements of stakeholders, while maintaining the integrity of the data. In this paper we critically examine the monitoring program for the Australian fur seal (AFS) Arctocephalus pusillus doriferus as an example of an ad-hoc monitoring program that was co-ordinated across multiple stakeholders as a range-wide census of live pups in the Austral summers of 2002, 2007 and 2013. This 5-yearly census, combined with historic counts at individual sites, successfully tracked increasing population trends as signs of population recovery up to 2007. The 2013 census identified the first reduction in AFS pup numbers (14,248 live pups, -4.2% change per annum since 2007), however we have limited information to understand this change. We analyse the trends at breeding colonies and perform a power analysis to critically examine the reliability of those trends. We then assess the gaps in the monitoring program and discuss how we may transition this surveillance style program to an adaptive monitoring program than can evolve over time and achieve its goals. The census results are used for ecosystem-based modelling for fisheries management and emergency response planning. The ultimate goal for this program is to obtain the data we need with minimal cost, effort and impact on the fur seals. In conclusion we identify the importance of power analyses for interpreting trends, the value of regularly assessing long-term monitoring programs and proper design so that adaptive monitoring principles can be applied.

Echoes from the past: Regional variations in recovery within a harbour seal population.

Terrestrial and marine wildlife populations have been severely reduced by hunting, fishing and habitat destruction, especially in the last centuries. Although management regulations have led to the recovery of some populations, the underlying processes are not always well understood. This study uses a 40-year time series of counts of harbour seals (Phoca vitulina) in the Wadden Sea to study these processes, and demonstrates the influence of historical regional differences in management regimes on the recovery of this population. While the Wadden Sea is considered one ecologically coupled zone, with a distinct harbour seal population, the area is divided into four geo-political regions i.e. the Netherlands, Lower Saxony including Hamburg, Schleswig-Holstein and Denmark. Gradually, seal hunting was banned between 1962 and 1977 in the different regions. Counts of moulting harbour seals and pup counts, obtained during aerial surveys between 1974 and 2014, show a population growth from approximately 4500 to 39,000 individuals. Population growth models were developed to assess if population growth differed between regions, taking into account two Phocine Distemper Virus (PDV) epizootics, in 1988 and 2002 which seriously affected the population. After a slow start prior to the first epizootic, the overall population grew exponentially at rates close to assumed maximum rates of increase in a harbour seal population. Recently, growth slowed down, potentially indicative of approaching carrying capacity. Regional differences in growth rates were demonstrated, with the highest recovery in Netherlands after the first PDV epizootic (i.e. 17.9%), suggesting that growth was fuelled by migration from the other regions, where growth remained at or below the intrinsic growth rate (13%). The seals' distribution changed, and although the proportion of seals counted in the German regions declined, they remained by far the most important pupping region, with approximately 70% of all pups being born there. It is hypothesised that differences in hunting regime, preceding the protection in the 1960's and 1970's, created unbalance in the distribution of breeding females throughout the Wadden Sea, which prevailed for decades. Breeding site fidelity promoted the growth in pup numbers at less affected breeding sites, while recolonisation of new breeding areas would be suppressed by the philopatry displayed by the animals born there. This study shows that for long-lived species, variable management regimes in this case hunting regulations, across a species' range can drive population dynamics for several generations.

Drivers and annual estimates of marine wildlife entanglement rates: A long-term case study with Australian fur seals.

Methods of calculating wildlife entanglement rates are not standardised between studies and often ignore the influence of observer effort, confounding comparisons. From 1997-2013 we identified 359 entangled Australian fur seals at Seal Rocks, south-eastern Australia. Most entanglement materials originated from commercial fisheries; most frequently entangling pups and juveniles. Using Generalized Additive Mixed Models, which incorporated observer effort and survey frequency, we identified that entanglements were observed more frequently amongst pups from July to October as they approached weaning. Neither the decline in regional fishing intensity nor changing seal population size influenced the incidence of entanglements. Using the models, we estimated that 302 (95% CI=182-510) entangled seals were at Seal Rocks each year, equivalent to 1.0% (CI=0.6-1.7%) of the site population. This study highlights the influence of observer effort and the value of long-term datasets for determining the drivers of marine debris entanglements.

Serologic survey for potential pathogens and assessment of disease risk in Australian fur seals.

The introduction of pathogens into populations of animals with no previous exposure to them and, therefore, no immunologic protection, can result in epizootics. Predicting the susceptibility of populations to infectious diseases is crucial for their conservation and management. Australian fur seals (Arctocephalus pusillus doriferus) have a relatively small population size, a restricted range, and form dense aggregations. These factors make this species vulnerable to epizootics of infectious diseases that spread by direct animal-to-animal contact. Blood samples were collected from 125 adult female Australian fur seals between 2007 and 2009 and tested for exposure to selected pathogens. The testing protocol was based on pathogens important to marine mammal health or those significant to public and livestock health. No antibodies were detected to morbilliviruses, influenza A viruses, six Leptospira serovars, Mycobacterium tuberculosis-complex species, or Toxoplasma gondii. Overall antibody prevalence to an unidentified Brucella sp. was 57% but varied significantly (P<0.02) between 2007 (74%) and 2008 (53%). The findings indicate Brucella infection may be enzootic in the Australian fur seal population. Further investigations are required to isolate the bacteria and establish if infection results in morbidity and mortality. Australian fur seals remain vulnerable to the threat of introduced disease and should be managed and monitored accordingly.

Mycoplasmas in Australian fur seals (Arctocephalus pusillus doriferus): identification and association with abortion.

Bacteria from the genus Mycoplasma are common inhabitants of the respiratory, gastrointestinal, and genital tracts of mammals. The understanding of the pathological significance of mycoplasmas in seals is poor, as few studies have utilized the specific culture techniques required to isolate these bacteria. The current study surveyed for the Mycoplasma species present in Australian fur seals (Arctocephalus pusillus doriferus) and investigated the association between infection and pathology. Mycoplasmas were found in the nasal cavities of 55/80 (69%) of apparently healthy individuals. Isolates from 18 individuals were investigated through 16S ribosomal RNA sequencing, and 3 species were identified: M. zalophi, M. phocae, and Mycoplasma sp. (GenBank no. EU714238.1), all of which had previously been isolated from Northern Hemisphere pinnipeds. In addition, mycoplasmas were isolated from the lungs of 4 out of 16 juveniles and 1 out of 5 adults sampled at necropsy. Isolates obtained were M. zalophi, Mycoplasma sp. EU714238.1, and M. phocicerebrale, but infection was not associated with lung pathology in these age classes. Inflammatory disease processes of the heart and/or lungs were present in 12 out of 32 (38%) aborted fetuses on microscopic examination. Predominant findings were interstitial pneumonia, pericarditis, and myocarditis. Mycoplasma phocicerebrale was isolated from the thymus of an aborted fetus, and 3 out of 11 (27%) fetuses with inflammatory heart or lung lesions were PCR-positive for Mycoplasma. In conclusion, several species of Mycoplasma are part of the normal flora of the nasal cavity of Australian fur seals, and some mycoplasmas may be associated with abortion in this species of seal.

Epizootiology of Brucella infection in Australian fur seals.

Novel members of the bacterial genus Brucella have recently emerged as pathogens of various marine mammal species and as potential zoonotic agents. We investigated the epizootiology of Brucella infection in Australian fur seals (Arctocephalus pusillus doriferus) by establishing demographic and temporal variations in antibody prevalence, attempting isolation of the causative agent, and determining whether this potential pathogen is involved in frequent abortions observed in this pinniped species. Two competitive enzyme-linked immunosorbent assays (cELISAs), an indirect ELISA, and a fluorescence polarization assay (FPA) were used to test sera for Brucella antibodies. The FPA and cELISA proved suitable for use in this species. Significant differences in antibody prevalence were found between age classes of seals sampled between 2007 and 2009 at one colony. Pups sampled at this site (n=134) were negative for Brucella antibodies by all serologic tests but 17 of 45 (38%) of juveniles were antibody-positive. Antibody prevalence in adult females was significantly higher than in juveniles (P=0.044). Antibody prevalence for adult females between 2003 and 2009 varied significantly over time (P=0.011), and for individuals sampled between 2003 and 2005, the likelihood of pregnancy was greater in individuals positive for Brucella antibodies (P=0.034). Inflammatory lesions suggestive of infectious agents were found in 14 of 39 aborted Australian fur seal pups, but pathologic changes were not uniformly consistent for Brucella infection. Culture and PCR investigations on fetal tissues were negative for Brucella. Culture and PCR on selected fresh or frozen tissues from 36 juvenile and adult animals were also negative. We suspect that the prevalence of active infection with Brucella in Australian fur seals is low relative to antibody prevalence.