Additive effects of climate and fisheries drive ongoing declines in multiple albatross species.

Environmental and anthropogenic factors often drive population declines in top predators, but how their influences may combine remains unclear. Albatrosses are particularly threatened. They breed in fast-changing environments, and their extensive foraging ranges expose them to incidental mortality (bycatch) in multiple fisheries. The albatross community at South Georgia includes globally important populations of three species that have declined by 40-60% over the last 35 years. We used three steps to deeply understand the drivers of such dramatic changes: (i) describe fundamental demographic rates using multievent models, (ii) determine demographic drivers of population growth using matrix models, and (iii) identify environmental and anthropogenic drivers using ANOVAs. Each species was affected by different processes and threats in their foraging areas during the breeding and nonbreeding seasons. There was evidence for two kinds of combined environmental and anthropogenic effects. The first was sequential; in wandering and black-browed albatrosses, high levels of bycatch have reduced juvenile and adult survival, then increased temperature, reduced sea-ice cover, and stronger winds are affecting the population recovery potential. The second was additive; in gray-headed albatrosses, not only did bycatch impact adult survival but also this impact was exacerbated by lower food availability in years following El Niño events. This emphasizes the need for much improved implementation of mitigation measures in fisheries and better enforcement of compliance. We hope our results not only help focus future management actions for these populations but also demonstrate the power of the modelling approach for assessing impacts of environmental and anthropogenic drivers in wild animal populations.

Sex-specific effects of fisheries and climate on the demography of sexually dimorphic seabirds.

Many animal taxa exhibit sex-specific variation in ecological traits, such as foraging and distribution. These differences could result in sex-specific responses to change, but such demographic effects are poorly understood. Here, we test for sex-specific differences in the demography of northern (NGP, Macronectes halli) and southern (SGP, M. giganteus) giant petrels - strongly sexually size-dimorphic birds that breed sympatrically at South Georgia, South Atlantic Ocean. Both species feed at sea or on carrion on land, but larger males (30% heavier) are more reliant on terrestrial foraging than the more pelagic females. Using multi-event mark-recapture models, we examine the impacts of long-term changes in environmental conditions and commercial fishing on annual adult survival and use two-sex matrix population models to forecast future trends. As expected, survival of male NGP was positively affected by carrion availability, but negatively affected by zonal winds. Female survival was positively affected by meridional winds and El Niño-Southern Oscillation (ENSO), and negatively affected by sea ice concentration and pelagic longline effort. Survival of SGPs did not differ between sexes; however, survival of males only was positively correlated with the Southern Annular Mode (SAM). Two-sex population projections indicate that future environmental conditions are likely to benefit giant petrels. However, any potential increase in pelagic longline fisheries could reduce female survival and population growth. Our study reveals that sex-specific ecological differences can lead to divergent responses to environmental drivers (i.e. climate and fisheries). Moreover, because such effects may not be apparent when all individuals are considered together, ignoring sex differences could underestimate the relative influence of a changing environment on demography.

Why is the South Orkney Island shelf (the world's first high seas marine protected area) a carbon immobilization hotspot?

The Southern Ocean archipelago, the South Orkney Islands (SOI), became the world's first entirely high seas marine protected area (MPA) in 2010. The SOI continental shelf (~44 000 km(2) ), was less than half covered by grounded ice sheet during glaciations, is biologically rich and a key area of both sea surface warming and sea-ice losses. Little was known of the carbon cycle there, but recent work showed it was a very important site of carbon immobilization (net annual carbon accumulation) by benthos, one of the few demonstrable negative feedbacks to climate change. Carbon immobilization by SOI bryozoans was higher, per species, unit area and ice-free day, than anywhere-else polar. Here, we investigate why carbon immobilization has been so high at SOI, and whether this is due to high density, longevity or high annual production in six study species of bryozoans (benthic suspension feeders). We compared benthic carbon immobilization across major regions around West Antarctica with sea-ice and primary production, from remotely sensed and directly sampled sources. Lowest carbon immobilization was at the northernmost study regions (South Georgia) and southernmost Amundsen Sea. However, data standardized for age and density showed that only SOI was anomalous (high). High immobilization at SOI was due to very high annual production of bryozoans (rather than high densities or longevity), which were 2x, 3x and 5x higher than on the Bellingshausen, South Georgia and Amundsen shelves, respectively. We found that carbon immobilization correlated to the duration (but not peak or integrated biomass) of phytoplankton blooms, both in directly sampled, local scale data and across regions using remote-sensed data. The long bloom at SOI seems to drive considerable carbon immobilization, but sea-ice losses across West Antarctica mean that significant carbon sinks and negative feedbacks to climate change could also develop in the Bellingshausen and Amundsen seas.

Assessing the effectiveness of specially protected areas for conservation of Antarctica's botanical diversity.

Vegetation is sparsely distributed over Antarctica's ice-free ground, and distinct plant communities are present in each of the continent's 15 recently identified Antarctic Conservation Biogeographic Regions (ACBRs). With rapidly increasing human activity in Antarctica, terrestrial plant communities are at risk of damage or destruction by trampling, overland transport, and infrastructure construction and from the impacts of anthropogenically introduced species, as well as uncontrollable pressures such as fur seal (Arctocephalus gazella) activity and climate change. Under the Protocol on Environmental Protection to the Antarctic Treaty, the conservation of plant communities can be enacted and facilitated through the designation of Antarctic Specially Protected Areas (ASPAs). We examined the distribution within the 15 ACBRs of the 33 ASPAs whose explicit purpose includes protecting macroscopic terrestrial flora. We completed the first survey using normalized difference vegetation index (NDVI) satellite remote sensing to provide baseline data on the extent of vegetation cover in all ASPAs designated for plant protection in Antarctica. Large omissions in the protection of Antarctic botanical diversity were found. There was no protection of plant communities in 6 ACBRs, and in another 6, <0.4% of the ACBR area was included in an ASPA that protected vegetation. Protected vegetation cover within the 33 ASPAs totaled 16.1 km(2) for the entire Antarctic continent; over half was within a single protected area. Over 96% of the protected vegetation was contained in 2 ACBRs, which together contributed only 7.8% of the continent's ice-free ground. We conclude that Antarctic botanical diversity is clearly inadequately protected and call for systematic designation of ASPAs protecting plant communities by the Antarctic Treaty Consultative Parties, the members of the governing body of the continent.

Climate Mitigation through Biological Conservation: Extensive and Valuable Blue Carbon Natural Capital in Tristan da Cunha's Giant Marine Protected Zone.

Carbon-rich habitats can provide powerful climate mitigation if meaningful protection is put in place. We attempted to quantify this around the Tristan da Cunha archipelago Marine Protected Area. Its shallows (<1000 m depth) are varied and productive. The 5.4 km2 of kelp stores ~60 tonnes of carbon (tC) and may export ~240 tC into surrounding depths. In deep-waters we analysed seabed data collected from three research cruises, including seabed mapping, camera imagery, seabed oceanography and benthic samples from mini-Agassiz trawl. Rich biological assemblages on seamounts significantly differed to the islands and carbon storage had complex drivers. We estimate ~2.3 million tC are stored in benthic biodiversity of waters <1000 m, which includes >0.22 million tC that can be sequestered (the proportion of the carbon captured that is expected to become buried in sediment or locked away in skeletal tissue for at least 100 years). Much of this carbon is captured by cold-water coral reefs as a mixture of inorganic (largely calcium carbonate) and organic compounds. As part of its 2020 Marine Protection Strategy, these deep-water reef systems are now protected by a full bottom-trawling ban throughout Tristan da Cunha and representative no take areas on its seamounts. This small United Kingdom Overseas Territory's reef systems represent approximately 0.8 Mt CO2 equivalent sequestered carbon; valued at >£24 Million GBP (at the UN shadow price of carbon). Annual productivity of this protected standing stock generates an estimated £3 million worth of sequestered carbon a year, making it an unrecognized and potentially major component of the economy of small island nations like Tristan da Cunha. Conservation of near intact habitats are expected to provide strong climate and biodiversity returns, which are exemplified by this MPA.

Long-term changes in habitat and trophic level of Southern Ocean squid in relation to environmental conditions.

Long-term studies of pelagic nekton in the Southern Ocean and their responses to ongoing environmental change are rare. Using stable isotope ratios measured in squid beaks recovered from diet samples of wandering albatrosses Diomedea exulans, we assessed decadal variation (from 1976 to 2016) in the habitat (δ13C) and trophic level (δ15N) of five important Southern Ocean squid species in relation to indices of environmental conditions-Southern Oscillation Index (SOI) and Southern Annular Mode (SAM). Based on δ13C values, corrected for the Suess effect, habitat had changed over the last 50 years for Taonius sp. B (Voss), Gonatus antarcticus, Galiteuthis glacialis and Histioteuthis atlantica but not Moroteuthopsis longimana. By comparison, mean δ15N values were similar across decades for all five species, suggesting minimal changes in trophic levels. Both SAM and SOI have increased in strength and frequency over the study period but, of the five species, only in Taonius sp. B (Voss) did these indices correlate with, δ13C and δ15N values, indicating direct relationships between environmental conditions, habitat and trophic level. The five cephalopod species therefore changed their habitats with changing environmental conditions over the last 50 years but maintained similar trophic levels. Hence, cephalopods are likely to remain important prey for top predators in Southern Ocean food webs, despite ongoing climate change.

Past penguin colony responses to explosive volcanism on the Antarctic Peninsula.

Changes in penguin populations on the Antarctic Peninsula have been linked to several environmental factors, but the potentially devastating impact of volcanic activity has not been considered. Here we use detailed biogeochemical analyses to track past penguin colony change over the last 8,500 years on Ardley Island, home to one of the Antarctic Peninsula's largest breeding populations of gentoo penguins. The first sustained penguin colony was established on Ardley Island c. 6,700 years ago, pre-dating sub-fossil evidence of Peninsula-wide occupation by c. 1,000 years. The colony experienced five population maxima during the Holocene. Overall, we find no consistent relationships with local-regional atmospheric and ocean temperatures or sea-ice conditions, although the colony population maximum, c. 4,000-3,000 years ago, corresponds with regionally elevated temperatures. Instead, at least three of the five phases of penguin colony expansion were abruptly ended by large eruptions from the Deception Island volcano, resulting in near-complete local extinction of the colony, with, on average, 400-800 years required for sustainable recovery.

Proximate drivers of spatial segregation in non-breeding albatrosses.

Many animals partition resources to avoid competition, and in colonially-breeding species this often leads to divergent space or habitat use. During the non-breeding season, foraging constraints are relaxed, yet the patterns and drivers of segregation both between and within populations are poorly understood. We modelled habitat preference to examine how extrinsic (habitat availability and intra-specific competition) and intrinsic factors (population, sex and breeding outcome) influence the distributions of non-breeding grey-headed albatrosses Thalassarche chrysostoma tracked from two major populations, South Georgia (Atlantic Ocean) and the Prince Edward Islands (Indian Ocean). Spatial segregation was greater than expected, reflecting distinct seasonal differences in habitat selection and accessibility, and avoidance of intra-specific competition with local breeders. Previously failed birds segregated spatially from successful birds during summer, when they used less productive waters, suggesting a link between breeding outcome and subsequent habitat selection. In contrast, we found weak evidence of sexual segregation, which did not reflect a difference in habitat use. Our results indicate that the large-scale spatial structuring of albatross distributions results from interactions between extrinsic and intrinsic factors, with important implications for population dynamics. As habitat preferences differed substantially between colonies, populations should be considered independently when identifying critical areas for protection.