Ship traffic connects Antarctica's fragile coasts to worldwide ecosystems.

Antarctica, an isolated and long considered pristine wilderness, is becoming increasingly exposed to the negative effects of ship-borne human activity, and especially the introduction of invasive species. Here, we provide a comprehensive quantitative analysis of ship movements into Antarctic waters and a spatially explicit assessment of introduction risk for nonnative marine species in all Antarctic waters. We show that vessels traverse Antarctica's isolating natural barriers, connecting it directly via an extensive network of ship activity to all global regions, especially South Atlantic and European ports. Ship visits are more than seven times higher to the Antarctic Peninsula (especially east of Anvers Island) and the South Shetland Islands than elsewhere around Antarctica, together accounting for 88% of visits to Southern Ocean ecoregions. Contrary to expectations, we show that while the five recognized "Antarctic Gateway cities" are important last ports of call, especially for research and tourism vessels, an additional 53 ports had vessels directly departing to Antarctica from 2014 to 2018. We identify ports outside Antarctica where biosecurity interventions could be most effectively implemented and the most vulnerable Antarctic locations where monitoring programs for high-risk invaders should be established.

Behavioural and physiological impacts of low salinity on the sea urchin Echinus esculentus.

Reduced seawater salinity as a result of freshwater input can exert a major influence on the ecophysiology of benthic marine invertebrates, such as echinoderms. While numerous experimental studies have explored the physiological and behavioural effects of short-term, acute exposure to low salinity in echinoids, surprisingly few have investigated the consequences of chronic exposure, or compared the two. In this study, the European sea urchin, Echinus esculentus, was exposed to low salinity over the short term (11‰, 16‰, 21‰, 26‰ and 31‰ for 24 h) and longer term (21, 26 and 31‰ for 25 days). Over the short term, oxygen consumption, activity coefficient and coelomic fluid osmolality were directly correlated with reduced salinity, with 100% survival at ≥21‰ and 0% at ≤16‰. Over the longer term at 21‰ (25 days), oxygen consumption was significantly higher, feeding was significantly reduced and activity coefficient values were significantly lower than at control salinity (31‰). At 26‰, all metrics were comparable to the control by the end of the experiment, suggesting acclimation. Furthermore, beneficial functional resistance (righting ability and metabolic capacity) to acute low salinity was observed at 26‰. Osmolality values were slightly hyperosmotic to the external seawater at all acclimation salinities, while coelomocyte composition and concentration were unaffected by chronic low salinity. Overall, E. esculentus demonstrate phenotypic plasticity that enables acclimation to reduced salinity around 26‰; however, 21‰ represents a lower acclimation threshold, potentially limiting its distribution in coastal areas prone to high freshwater input.

A comparative study of tissue protein synthesis rates in an Antarctic, Harpagifer antarcticus and a temperate, Lipophrys pholis teleost.

The affect of temperature on tissue protein synthesis rates has been reported in temperate and tropical, but not Antarctic fishes. Previous studies have generally demonstrated low growth rates in Antarctic fish species in comparison to temperate relatives and elevated levels of protein turnover. This study investigates how low temperatures effect tissue protein synthesis and hence tissue growth in a polar fish species. Groups of Antarctic, Harpagifer antarcticus and temperate, Lipophrys pholis, were acclimated to a range of overlapping water temperatures and protein synthesis was measure in white muscle (WM), liver and gastrointestinal tract (GIT). WM protein synthesis rates increased linearly with temperature in both species (H. antarcticus 0.16-0.23%.d-1, L. pholis, 0.31-0.76%.d-1), while liver (H. antarcticus 0.24-0.27%.d-1, L. pholis, 0.44-1.03%.d-1) and GIT were unaffected by temperature in H. antarcticus but increased non-linearly in L.pholis (H. antarcticus 0.22-0.26%.d-1, L. pholis, 0.40-0.86%.d-1). RNA to protein ratios were unaffected by temperature in H. antarcticus but increased weakly, in L.pholis WM and liver. In L.pholis, RNA translational efficiency increased significantly with temperature in all tissues, but only in liver in H. antarcticus. At the overlapping temperature of 3 °C, protein synthesis (WM 26%, Liver, 39%, GIT, 35%) and RNA translational efficiency (WM 273%, Liver, 271%, GIT, 300%) were significantly lower in H. antarcticus than L.pholis, while RNA to protein ratios were significantly higher (WM 270%, Liver 170%, GIT 186%). Tissue specific effects of temperature are detectable in both species. This study provides the first evidence, that tissue protein synthesis rates are constrained in Antarctic fishes.

Can Antarctica's shallow zoobenthos 'bounce back' from iceberg scouring impacts driven by climate change?

All coastal systems experience disturbances and many across the planet are under unprecedented threat from an intensification of a variety of stressors. The West Antarctic Peninsula is a hotspot of physical climate change and has experienced a dramatic loss of sea-ice and glaciers in recent years. Among other things, sea-ice immobilizes icebergs, reducing collisions between icebergs and the seabed, thus decreasing ice-scouring. Ice disturbance drives patchiness in successional stages across seabed assemblages in Antarctica's shallows, making this an ideal system to understand the ecosystem resilience to increasing disturbance with climate change. We monitored a shallow benthic ecosystem before, during and after a 3-year pulse of catastrophic ice-scouring events and show that such systems can return, or bounce back, to previous states within 10 years. Our long-term data series show that recovery can happen more rapidly than expected, when disturbances abate, even in highly sensitive cold, polar environments.

A century of coping with environmental and ecological changes via compensatory biomineralization in mussels.

Accurate biological models are critical to predict biotic responses to climate change and human-caused disturbances. Current understanding of organismal responses to change stems from studies over relatively short timescales. However, most projections lack long-term observations incorporating the potential for transgenerational phenotypic plasticity and genetic adaption, the keys to resistance. Here, we describe unexpected temporal compensatory responses in biomineralization as a mechanism for resistance to altered environmental conditions and predation impacts in a calcifying foundation species. We evaluated exceptional archival specimens of the blue mussel Mytilus edulis collected regularly between 1904 and 2016 along 15 km of Belgian coastline, along with records of key environmental descriptors and predators. Contrary to global-scale predictions, shell production increased over the last century, highlighting a protective capacity of mussels for qualitative and quantitative trade-offs in biomineralization as compensatory responses to altered environments. We also demonstrated the role of changes in predator communities in stimulating unanticipated biological trends that run contrary to experimental predictive models under future climate scenarios. Analysis of archival records has a key role for anticipating emergent impacts of climate change.

Legacy and Emerging Persistent Organic Pollutants in Antarctic Benthic Invertebrates near Rothera Point, Western Antarctic Peninsula.

Pollutant levels in polar regions are gaining progressively more attention from the scientific community. This is especially so for pollutants that persist in the environment and can reach polar latitudes via a wide range of routes, such as some persistent organic pollutants (POPs). In this study, samples of Antarctic marine benthic organisms were analyzed for legacy and emerging POPs (polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and organochlorine pesticides) to comprehensively assess their current POP concentrations and infer the potential sources of the pollutants. Specimens of five benthic invertebrate species were collected at two distinct locations near Rothera research station on the Antarctic Peninsula (67°35'8 ̋ S and 68°7'59 ̋ W). Any impact of the nearby Rothera station as a local source of pollution appeared to be negligible. The most abundant chemicals detected were hexachlorobenzene (HCB) and BDE-209. The highest concentrations detected were in limpets and sea urchins, followed by sea stars, ascidians, and sea cucumbers. The relative congener patterns of PCBs and PBDEs were similar in all of the species. Some chemicals (e.g., heptachlor, oxychlordane, and mirex) were detected in the Antarctic invertebrates for the first time. Statistical analyses revealed that the distribution of the POPs was not only driven by the feeding traits of the species but also by the physicochemical properties of the specific compounds.

Snow algae communities in Antarctica: metabolic and taxonomic composition.

Snow algae are found in snowfields across cold regions of the planet, forming highly visible red and green patches below and on the snow surface. In Antarctica, they contribute significantly to terrestrial net primary productivity due to the paucity of land plants, but our knowledge of these communities is limited. Here we provide the first description of the metabolic and species diversity of green and red snow algae communities from four locations in Ryder Bay (Adelaide Island, 68°S), Antarctic Peninsula. During the 2015 austral summer season, we collected samples to measure the metabolic composition of snow algae communities and determined the species composition of these communities using metabarcoding. Green communities were protein-rich, had a high chlorophyll content and contained many metabolites associated with nitrogen and amino acid metabolism. Red communities had a higher carotenoid content and contained more metabolites associated with carbohydrate and fatty acid metabolism. Chloromonas, Chlamydomonas and Chlorella were found in green blooms but only Chloromonas was detected in red blooms. Both communities also contained bacteria, protists and fungi. These data show the complexity and variation within snow algae communities in Antarctica and provide initial insights into the contribution they make to ecosystem functioning.

Antarctica: The final frontier for marine biological invasions.

Antarctica is experiencing significant ecological and environmental change, which may facilitate the establishment of non-native marine species. Non-native marine species will interact with other anthropogenic stressors affecting Antarctic ecosystems, such as climate change (warming, ocean acidification) and pollution, with irreversible ramifications for biodiversity and ecosystem services. We review current knowledge of non-native marine species in the Antarctic region, the physical and physiological factors that resist establishment of non-native marine species, changes to resistance under climate change, the role of legislation in limiting marine introductions, and the effect of increasing human activity on vectors and pathways of introduction. Evidence of non-native marine species is limited: just four marine non-native and one cryptogenic species that were likely introduced anthropogenically have been reported freely living in Antarctic or sub-Antarctic waters, but no established populations have been reported; an additional six species have been observed in pathways to Antarctica that are potentially at risk of becoming invasive. We present estimates of the intensity of ship activity across fishing, tourism and research sectors: there may be approximately 180 vessels and 500+ voyages in Antarctic waters annually. However, these estimates are necessarily speculative because relevant data are scarce. To facilitate well-informed policy and management, we make recommendations for future research into the likelihood of marine biological invasions in the Antarctic region.

Biomineralization plasticity and environmental heterogeneity predict geographical resilience patterns of foundation species to future change.

Although geographical patterns of species' sensitivity to environmental changes are defined by interacting multiple stressors, little is known about compensatory processes shaping regional differences in organismal vulnerability. Here, we examine large-scale spatial variations in biomineralization under heterogeneous environmental gradients of temperature, salinity and food availability across a 30° latitudinal range (3,334 km), to test whether plasticity in calcareous shell production and composition, from juveniles to large adults, mediates geographical patterns of resilience to climate change in critical foundation species, the mussels Mytilus edulis and M. trossulus. We find shell calcification decreased towards high latitude, with mussels producing thinner shells with a higher organic content in polar than temperate regions. Salinity was the best predictor of within-region differences in mussel shell deposition, mineral and organic composition. In polar, subpolar, and Baltic low-salinity environments, mussels produced thin shells with a thicker external organic layer (periostracum), and an increased proportion of calcite (prismatic layer, as opposed to aragonite) and organic matrix, providing potentially higher resistance against dissolution in more corrosive waters. Conversely, in temperate, higher salinity regimes, thicker, more calcified shells with a higher aragonite (nacreous layer) proportion were deposited, which suggests enhanced protection under increased predation pressure. Interacting effects of salinity and food availability on mussel shell composition predict the deposition of a thicker periostracum and organic-enriched prismatic layer under forecasted future environmental conditions, suggesting a capacity for increased protection of high-latitude populations from ocean acidification. These findings support biomineralization plasticity as a potentially advantageous compensatory mechanism conferring Mytilus species a protective capacity for quantitative and qualitative trade-offs in shell deposition as a response to regional alterations of abiotic and biotic conditions in future environments. Our work illustrates that compensatory mechanisms, driving plastic responses to the spatial structure of multiple stressors, can define geographical patterns of unanticipated species resilience to global environmental change.

Thicker Shells Compensate Extensive Dissolution in Brachiopods under Future Ocean Acidification.

Organisms with long generation times require phenotypic plasticity to survive in changing environments until genetic adaptation can be achieved. Marine calcifiers are particularly vulnerable to ocean acidification due to dissolution and a reduction in shell-building carbonate ions. Long-term experiments assess organisms' abilities to acclimatize or even adapt to environmental change. Here we present an unexpected compensatory response to extensive shell dissolution in a highly calcium-carbonate-dependent organism after long-term culture in predicted end-century acidification and warming conditions. Substantial shell dissolution with decreasing pH posed a threat to both a polar ( Liothyrella uva) and a temperate ( Calloria inconspicua) brachiopod after 7 months and 3 months exposure, respectively, with more extensive dissolution in the polar species. This impact was reflected in decreased outer primary layer thickness in the polar brachiopod. A compensatory response of increasing inner secondary layer thickness, and thereby producing a thicker shell, was exhibited by the polar species. Less extensive dissolution in the temperate brachiopod did not affect shell thickness. Increased temperature did not impact shell dissolution or thickness. Brachiopod ability to produce a thicker shell when extensive shell dissolution occurs suggests this marine calcifier has great plasticity in calcification providing insights into how similar species might cope under future environmental change.

Spatial and temporal dynamics of Antarctic shallow soft-bottom benthic communities: ecological drivers under climate change.

BACKGROUND: Marine soft sediments are some of the most widespread habitats in the ocean, playing a vital role in global carbon cycling, but are amongst the least studied with regard to species composition and ecosystem functioning. This is particularly true of the Polar Regions, which are currently undergoing rapid climate change, the impacts of which are poorly understood. Compared to other latitudes, Polar sediment habitats also experience additional environmental drivers of strong seasonality and intense disturbance from iceberg scouring, which are major structural forces for hard substratum communities. This study compared sediment assemblages from two coves, near Rothera Point, Antarctic Peninsula, 67°S in order to understand the principal drivers of community structure, for the first time, evaluating composition across all size classes from mega- to micro-fauna. RESULTS: Morpho-taxonomy identified 77 macrofaunal species with densities of 464-16,084 individuals m-2. eDNA metabarcoding of microfauna, in summer only, identified a higher diversity, 189 metazoan amplicon sequence variants (ASVs) using the 18S ribosomal RNA and 249 metazoan ASVs using the mitochondrial COI gene. Both techniques recorded a greater taxonomic diversity in South Cove than Hangar Cove, with differences in communities between the coves, although the main taxonomic drivers varied between techniques. Morphotaxonomy identified the main differences between coves as the mollusc, Altenaeum charcoti, the cnidarian Edwardsia sp. and the polychaetes from the family cirratulidae. Metabarcoding identified greater numbers of species of nematodes, crustaceans and Platyhelminthes in South Cove, but more bivalve species in Hangar Cove. There were no detectable differences in community composition, measured through morphotaxonomy, between seasons, years or due to iceberg disturbance. CONCLUSIONS: This study found that unlike hard substratum communities the diversity of Antarctic soft sediment communities is correlated with the same factors as other latitudes. Diversity was significantly correlated with grain size and organic content, not iceberg scour. The increase in glacial sediment input as glaciers melt, may therefore be more important than increased iceberg disturbance.

A 120-year record of resilience to environmental change in brachiopods.

The inability of organisms to cope in changing environments poses a major threat to their survival. Rising carbon dioxide concentrations, recently exceeding 400 µatm, are rapidly warming and acidifying our oceans. Current understanding of organism responses to this environmental phenomenon is based mainly on relatively short- to medium-term laboratory and field experiments, which cannot evaluate the potential for long-term acclimation and adaptation, the processes identified as most important to confer resistance. Here, we present data from a novel approach that assesses responses over a centennial timescale showing remarkable resilience to change in a species predicted to be vulnerable. Utilising museum collections allows the assessment of how organisms have coped with past environmental change. It also provides a historical reference for future climate change responses. We evaluated a unique specimen collection of a single species of brachiopod (Calloria inconspicua) collected every decade from 1900 to 2014 from one sampling site. The majority of brachiopod shell characteristics remained unchanged over the past century. One response, however, appears to reinforce their shell by constructing narrower punctae (shell perforations) and laying down more shell. This study indicates one of the most calcium-carbonate-dependent species globally to be highly resilient to environmental change over the last 120 years and provides a new insight for how similar species might react and possibly adapt to future change.

Biodiversity in marine invertebrate responses to acute warming revealed by a comparative multi-omics approach.

Understanding species' responses to environmental change underpins our abilities to make predictions on future biodiversity under any range of scenarios. In spite of the huge biodiversity in most ecosystems, a model species approach is often taken in environmental studies. To date, we still do not know how many species we need to study to input into models and inform on ecosystem-level responses to change. In this study, we tested current paradigms on factors setting thermal limits by investigating the acute warming response of six Antarctic marine invertebrates: a crustacean Paraceradocus miersi, a brachiopod Liothyrella uva, two bivalve molluscs, Laternula elliptica, Aequiyoldia eightsii, a gastropod mollusc Marseniopsis mollis and an echinoderm Cucumaria georgiana. Each species was warmed at the rate of 1 °C h-1 and taken to the same physiological end point (just prior to heat coma). Their molecular responses were evaluated using complementary metabolomics and transcriptomics approaches with the aim of discovering the underlying mechanisms of their resilience or sensitivity to warming. The responses were species-specific; only two showed accumulation of anaerobic end products and three exhibited the classical heat shock response with expression of HSP70 transcripts. These diverse cellular measures did not directly correlate with resilience to heat stress and suggested that each species may have a different critical point of failure. Thus, one unifying molecular mechanism underpinning response to warming could not be assigned, and no overarching paradigm was supported. This biodiversity in response makes future ecosystems predictions extremely challenging, as we clearly need to develop a macrophysiology-type approach to cellular evaluations of the environmental stress response, studying a range of well-rationalized members from different community levels and of different phylogenetic origins rather than extrapolating from one or two arbitrary model species.

Deciphering the molecular adaptation of the king scallop (Pecten maximus) to heat stress using transcriptomics and proteomics.

BACKGROUND: The capacity of marine species to survive chronic heat stress underpins their ability to survive warming oceans as a result of climate change. In this study RNA-Seq and 2-DE proteomics were employed to decipher the molecular response of the sub-tidal bivalve Pecten maximus, to elevated temperatures. RESULTS: Individuals were maintained at three different temperatures (15, 21 and 25 °C) for 56 days, representing control conditions, maximum environmental temperature and extreme warming, with individuals sampled at seven time points. The scallops thrived at 21 °C, but suffered a reduction in condition at 25 °C. RNA-Seq analyses produced 26,064 assembled contigs, of which 531 were differentially expressed, with putative annotation assigned to 177 transcripts. The proteomic approach identified 24 differentially expressed proteins, with nine identified by mass spectrometry. Network analysis of these results indicated a pivotal role for GAPDH and AP-1 signalling pathways. Data also suggested a remodelling of the cell structure, as revealed by the differential expression of genes involved in the cytoskeleton and cell membrane and a reduction in DNA repair. They also indicated the diversion of energetic metabolism towards the mobilization of lipid energy reserves to fuel the increased metabolic rate at the higher temperature. CONCLUSIONS: This work provides preliminary insights into the response of P. maximus to chronic heat stress and provides a basis for future studies examining the tipping points and energetic trade-offs of scallop culture in warming oceans.

Variability among individuals is generated at the gene expression level.

Selection acts on individuals, specifically on their differences. To understand adaptation and responses to change therefore requires knowledge of how variation is generated and distributed across traits. Variation occurs on different biological scales, from genetic through physiological to morphological, yet it is unclear which of these carries the most variability. For example, if individual variation is mainly generated by differences in gene expression, variability should decrease progressively from coding genes to morphological traits, whereas if post-translational and epigenetic effects increase variation, the opposite should occur. To test these predictions, we compared levels of variation among individuals in various measures of gene expression, physiology (including activity), and morphology in two abundant and geographically widespread Antarctic molluscs, the clam Laternula elliptica and the limpet Nacella concinna. Direct comparisons among traits as diverse as heat shock protein QPCR assays, whole transcription profiles, respiration rates, burying rate, shell length, and ash-free dry mass were made possible through the novel application of an established metric, the Wentworth Scale. In principle, this approach could be extended to analyses of populations, communities, or even entire ecosystems. We found consistently greater variation in gene expression than morphology, with physiological measures falling in between. This suggests that variability is generated at the gene expression level. These findings have important implications for refining current biological models and predictions of how biodiversity may respond to climate change.

Acidification effects on biofouling communities: winners and losers.

How ocean acidification affects marine life is a major concern for science and society. However, its impacts on encrusting biofouling communities, that are both the initial colonizers of hard substrata and of great economic importance, are almost unknown. We showed that community composition changed significantly, from 92% spirorbids, 3% ascidians and 4% sponges initially to 47% spirorbids, 23% ascidians and 29% sponges after 100 days in acidified conditions (pH 7.7). In low pH, numbers of the spirorbid Neodexiospira pseudocorrugata were reduced ×5 compared to controls. The two ascidians present behaved differently with Aplidium sp. decreasing ×10 in pH 7.7, whereas Molgula sp. numbers were ×4 higher in low pH than controls. Calcareous sponge (Leucosolenia sp.) numbers increased ×2.5 in pH 7.7 over controls. The diatom and filamentous algal community was also more poorly developed in the low pH treatments compared to controls. Colonization of new surfaces likewise showed large decreases in spirorbid numbers, but numbers of sponges and Molgula sp. increased. Spirorbid losses appeared due to both recruitment failure and loss of existing tubes. Spirorbid tubes are comprised of a loose prismatic fabric of calcite crystals. Loss of tube materials appeared due to changes in the binding matrix and not crystal dissolution, as SEM analyses showed crystal surfaces were not pitted or dissolved in low pH conditions. Biofouling communities face dramatic future changes with reductions in groups with hard exposed exoskeletons and domination by soft-bodied ascidians and sponges.

Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short-term exposures.

This study examined the effects of long-term culture under altered conditions on the Antarctic sea urchin, Sterechinus neumayeri. Sterechinus neumayeri was cultured under the combined environmental stressors of lowered pH (-0.3 and -0.5 pH units) and increased temperature (+2 °C) for 2 years. This time-scale covered two full reproductive cycles in this species and analyses included studies on both adult metabolism and larval development. Adults took at least 6-8 months to acclimate to the altered conditions, but beyond this, there was no detectable effect of temperature or pH. Animals were spawned after 6 and 17 months exposure to altered conditions, with markedly different outcomes. At 6 months, the percentage hatching and larval survival rates were greatest in the animals kept at 0 °C under current pH conditions, whilst those under lowered pH and +2 °C performed significantly less well. After 17 months, performance was not significantly different across treatments, including controls. However, under the altered conditions urchins produced larger eggs compared with control animals. These data show that under long-term culture adult S. neumayeri appear to acclimate their metabolic and reproductive physiology to the combined stressors of altered pH and increased temperature, with relatively little measureable effect. They also emphasize the importance of long-term studies in evaluating effects of altered pH, particularly in slow developing marine species with long gonad maturation times, as the effects of altered conditions cannot be accurately evaluated unless gonads have fully matured under the new conditions.

Acclimation and thermal tolerance in Antarctic marine ectotherms.

Antarctic marine species have evolved in one of the coldest and most temperature-stable marine environments on Earth. They have long been classified as being stenothermal, or having a poor capacity to resist warming. Here we show that their ability to acclimate their physiology to elevated temperatures is poor compared with species from temperate latitudes, and similar to those from the tropics. Those species that have been demonstrated to acclimate take a very long time to do so, with Antarctic fish requiring up to 21-36 days to acclimate, which is 2-4 times as long as temperate species, and invertebrates requiring between 2 and 5 months to complete whole-animal acclimation. Investigations of upper thermal tolerance (CT(max)) in Antarctic marine species have shown that as the rate of warming is reduced in experiments, CT(max) declines markedly, ranging from 8 to 17.5 °C across 13 species at a rate of warming of 1 °C day(-1), and from 1 to 6 °C at a rate of 1 °C month(-1). This effect of the rate of warming on CT(max) also appears to be present at all latitudes. A macrophysiological analysis of long-term CT(max) across latitudes for marine benthic groups showed that both Antarctic and tropical species were less resistant to elevated temperatures in experiments and thus had lower warming allowances (measured as the difference between long-term CT(max) and experienced environmental temperature), or warming resistance, than temperate species. This makes them more at risk from warming than species from intermediate latitudes. This suggests that the variability of environmental temperature may be a major factor in dictating an organism's responses to environmental change.