Quantifying pigment content in crustose coralline algae using hyperspectral imaging: A case study with Tethysphytum antarcticum (Ross Sea, Antarctica).

Crustose coralline algae (CCA) are a highly diverse group of habitat-forming, calcifying red macroalgae (Rhodophyta) with unique adaptations to diverse irradiance regimes. A distinctive CCA phenotype adaptation, which allows them to maximize photosynthetic performance in low light, is their content of a specific group of light-harvesting pigments called phycobilins. In this study, we assessed the potential of noninvasive hyperspectral imaging (HSI) in the visible spectrum (400-800 nm) to describe the phenotypic variability in phycobilin content of an Antarctic coralline, Tethysphytum antarcticum (Hapalidiales), from two distinct locations. We validated our measurements with pigment extractions and spectrophotometry analysis, in addition to DNA barcoding using the psbA marker. Targeted spectral indices were developed and correlated with phycobilin content using linear mixed models (R2 = 0.64-0.7). Once applied to the HSI, the models revealed the distinct phycoerythrin spatial distribution in the two site-specific CCA phenotypes, with thin and thick crusts, respectively. This study advances the capabilities of hyperspectral imaging as a tool to quantitatively study CCA pigmentation in relation to their phenotypic plasticity, which can be applied in laboratory studies and potentially in situ surveys using underwater hyperspectral imaging systems.

Sea Ice Dynamics Drive Benthic Microbial Communities in McMurdo Sound, Antarctica.

Climate change is driving dramatic variability in sea ice dynamics, a key driver in polar marine ecosystems. Projected changes in Antarctica suggest that regional warming will force dramatic shifts in sea ice thickness and persistence, altering sea ice-associated primary production and deposition to the seafloor. To improve our understanding of the impacts of sea ice change on benthic ecosystems, we directly compared the benthic microbial communities underlying first-year sea ice (FYI) and multi-year sea ice (MYI). Using two tractable coastal habitats in McMurdo Sound, Antarctica, where FYI (Cape Evans) and MYI (New Harbour) prevail, we show that the structure and composition of the benthic microbial communities reflect the legacy of sea ice dynamics. At Cape Evans, an enrichment of known heterotrophic algal polysaccharide degrading taxa (e.g., Flavobacteriaceae, unclassified Gammaproteobacteria, and Rubritaleaceae) and sulfate-reducing bacteria (e.g., Desulfocapsaceae) correlated with comparatively higher chlorophyll a (14.2±0.8µgg-1) and total organic carbon content (0.33%±0.04), reflecting increased productivity and seafloor deposition beneath FYI. Conversely, at New Harbour, an enrichment of known archaeal (e.g., Nitrosopumilaceae) and bacterial (e.g., Woeseiaceae and Nitrospiraceae) chemoautotrophs was common in sediments with considerably lower chlorophyll a (1.0±0.24µgg-1) and total organic carbon content (0.17%±0.01), reflecting restricted productivity beneath MYI. We also report evidence of a submarine discharge of sub-permafrost brine from Taylor Valley into New Harbour. By comparing our two study sites, we show that under current climate-warming scenarios, changes to sea ice productivity and seafloor deposition are likely to initiate major shifts in benthic microbial communities, with heterotrophic organic matter degradation processes becoming increasingly important. This study provides the first assessment of how legacy sea ice conditions influence benthic microbial communities in Antarctica, contributing insight into sea ice-benthic coupling and ecosystem functioning in a polar environment.

Climate cascades affect coastal Antarctic seafloor ecosystem functioning.

Polar seafloor ecosystems are changing rapidly and dramatically, challenging previously held paradigms of extreme dynamical stability. Warming-related declines in polar sea ice are expected to alter fluxes of phytoplankton and under-ice algae to the seafloor. Yet, how changes in food flux cascade through to seafloor communities and functions remains unclear. We leveraged natural spatial and temporal gradients in summertime sea ice extent to better understand the trajectories and implications of climate-related change in McMurdo Sound, Antarctica. McMurdo Sound was expected to be one of the last coastal marine environments on Earth to be affected by planetary warming, but the situation may be changing. Comparing satellite observations of selected coastal sites in McMurdo Sound between 2010-2017 and 2002-2009 revealed more ice-free days per year, and shorter distances to open water during the warmest months each year, in the more recent period. Interdecadal Pacific Oscillation (IPO), Oceanic Niño Index (ONI) and Antarctic Oscillation (AAO) climate indices peaked concurrently between 2014 and 2017 when sea ice breakouts in McMurdo Sound were most spatially and temporally extensive. Increases in sediment chlorophyll a and phaeophytin content (indicating increased deposition of detrital algal food material) were recorded during 2014-2017 at three coastal study sites in McMurdo Sound following the major sea ice breakouts. Soft-sediment seafloor ecosystem metabolism (measured in benthic incubation chambers as dissolved oxygen and inorganic nutrient fluxes) was correlated with sediment algal pigment concentration. Epifaunal invertebrate density, particularly opportunistic sessile suspension feeders, and infaunal community composition also shifted with increased food supply. The ecological characteristics and functions measured at the food-poor sites shifted towards those observed at richer sites at a surprisingly fast pace. These results indicate the sensitivity of the benthos and shed light on Antarctic marine trophic cascades and trajectories of response of iconic high-latitude seafloor habitats to a warming climate.

Antarctic ecosystems in transition - life between stresses and opportunities.

Important findings from the second decade of the 21st century on the impact of environmental change on biological processes in the Antarctic were synthesised by 26 international experts. Ten key messages emerged that have stakeholder-relevance and/or a high impact for the scientific community. They address (i) altered biogeochemical cycles, (ii) ocean acidification, (iii) climate change hotspots, (iv) unexpected dynamism in seabed-dwelling populations, (v) spatial range shifts, (vi) adaptation and thermal resilience, (vii) sea ice related biological fluctuations, (viii) pollution, (ix) endangered terrestrial endemism and (x) the discovery of unknown habitats. Most Antarctic biotas are exposed to multiple stresses and considered vulnerable to environmental change due to narrow tolerance ranges, rapid change, projected circumpolar impacts, low potential for timely genetic adaptation, and migration barriers. Important ecosystem functions, such as primary production and energy transfer between trophic levels, have already changed, and biodiversity patterns have shifted. A confidence assessment of the degree of 'scientific understanding' revealed an intermediate level for most of the more detailed sub-messages, indicating that process-oriented research has been successful in the past decade. Additional efforts are necessary, however, to achieve the level of robustness in scientific knowledge that is required to inform protection measures of the unique Antarctic terrestrial and marine ecosystems, and their contributions to global biodiversity and ecosystem services.

Responses of a common New Zealand coastal sponge to elevated suspended sediments: Indications of resilience.

Suspended sediments can affect the health of marine benthic suspension feeders, with concomitant effects on community diversity, abundance and ecosystem function. Suspended sediment loads can become elevated through trawling and dredging, and via resuspension of bottom sediments and/or direct input from land during storms. We assessed the functioning (survival, respiration, morphology) of a common New Zealand cushion sponge, Crella incrustans (Carter, 1885), during four weeks of exposure to a gradient of suspended sediment concentrations (SSC). Survival was high, and oxygen consumption was not affected. Sponges did, however, develop apical fistules, a phenomenon never-before observed in this species. Although sediments accumulated internally within the sponges, around a third had cleared these sediments two weeks after the elevated SSCs were removed. The environments these sponges inhabit may predispose them to coping with high SSCs. Such experiments are useful for defining SSC tolerances, which may influence how such impacts can be managed.

Effect of reduced pH on physiology and shell integrity of juvenile Haliotis iris (paua) from New Zealand.

The New Zealand paua or black footed abalone, Haliotis iris, is one of many mollusc species at potential risk from ocean acidification and warming. To investigate possible impacts, juvenile paua (~24 mm shell length) were grown for 4 months in seawater pH/pCO2 conditions projected for 2100. End of century seawater projections (pHT 7.66/pCO2 ~1,000 µatm) were contrasted with local ambient conditions (pHT 8.00/pCO2 ~400 µatm) at two typical temperatures (13 and 15 °C). We used a combination of methods (morphometric, scanning electron microscopy, X-ray diffraction) to investigate effects on juvenile survival and growth, as well as shell mineralogy and integrity. Lowered pH did not affect survival, growth rate or condition, but animals grew significantly faster at the higher temperature. Juvenile paua were able to biomineralise their inner nacreous aragonite layer and their outer prismatic calcite layer under end-of-century pH conditions, at both temperatures, and carbonate composition was not affected. There was some thickening of the nacre layer in the newly deposited shell with reduced pH and also at the higher temperature. Most obvious was post-depositional alteration of the shell under lowered pH: the prismatic calcite layer was thinner, and there was greater etching of the external shell surface; this dissolution was greater at the higher temperature. These results demonstrate the importance of even a small (2 °C) difference in temperature on growth and shell characteristics, and on modifying the effects at lowered pH. Projected CO2-related changes may affect shell quality of this iconic New Zealand mollusc through etching (dissolution) and thinning, with potential implications for resilience to physical stresses such as predation and wave action.

In situ response of Antarctic under-ice primary producers to experimentally altered pH.

Elevated atmospheric CO2 concentrations are contributing to ocean acidification (reduced seawater pH and carbonate concentrations), with potentially major ramifications for marine ecosystems and their functioning. Using a novel in situ experiment we examined impacts of reduced seawater pH on Antarctic sea ice-associated microalgal communities, key primary producers and contributors to food webs. pH levels projected for the following decades-to-end of century (7.86, 7.75, 7.61), and ambient levels (7.99), were maintained for 15 d in under-ice incubation chambers. Light, temperature and dissolved oxygen within the chambers were logged to track diurnal variation, with pH, O2, salinity and nutrients assessed daily. Uptake of CO2 occurred in all treatments, with pH levels significantly elevated in the two extreme treatments. At the lowest pH, despite the utilisation of CO2 by the productive microalgae, pH did not return to ambient levels and carbonate saturation states remained low; a potential concern for organisms utilising this under-ice habitat. However, microalgal community biomass and composition were not significantly affected and only modest productivity increases were noted, suggesting subtle or slightly positive effects on under-ice algae. This in situ information enables assessment of the influence of future ocean acidification on under-ice community characteristics in a key coastal Antarctic habitat.

The physiological response of the deep-sea coral Solenosmilia variabilis to ocean acidification.

Several forms of calcifying scleractinian corals provide important habitat complexity in the deep-sea and are consistently associated with a high biodiversity of fish and other invertebrates. How these corals may respond to the future predicted environmental conditions of ocean acidification is poorly understood, but any detrimental effects on these marine calcifiers will have wider impacts on the ecosystem. Colonies of Solenosmilia variabilis, a protected deep-sea coral commonly occurring throughout the New Zealand region, were collected during a cruise in March 2014 from the Louisville Seamount Chain. Over a 12-month period, samples were maintained in temperature controlled (∼3.5 °C) continuous flow-through tanks at a seawater pH that reflects the region's current conditions (7.88) and an end-of-century scenario (7.65). Impacts on coral growth and the intensity of colour saturation (as a proxy for the coenenchyme tissue that covers the coral exoskeleton and links the coral polyps) were measured bimonthly. In addition, respiration rate was measured after a mid-term (six months) and long-term (12 months) exposure period. Growth rates were highly variable, ranging from 0.53 to 3.068 mm year-1 and showed no detectable difference between the treatment and control colonies. Respiration rates also varied independently of pH and ranged from 0.065 to 1.756 µmol O2 g protein-1 h-1. A significant change in colour was observed in the treatment group over time, indicating a loss of coenenchyme. This loss was greatest after 10 months at 5.28% and could indicate a reallocation of energy with physiological processes (e.g.  growth and respiration) being maintained at the expense of coenenchyme production. This research illustrates important first steps to assessing and understanding the sensitivity of deep-sea corals to ocean acidification.

High resolution microscopy reveals significant impacts of ocean acidification and warming on larval shell development in Laternula elliptica.

Environmental stressors impact marine larval growth rates, quality and sizes. Larvae of the Antarctic bivalve, Laternula elliptica, were raised to the D-larvae stage under temperature and pH conditions representing ambient and end of century projections (-1.6°C to +0.4°C and pH 7.98 to 7.65). Previous observations using light microscopy suggested pH had no influence on larval abnormalities in this species. Detailed analysis of the shell using SEM showed that reduced pH is in fact a major stressor during development for this species, producing D-larvae with abnormal shapes, deformed shell edges and irregular hinges, cracked shell surfaces and even uncalcified larvae. Additionally, reduced pH increased pitting and cracking on shell surfaces. Thus, apparently normal larvae may be compromised at the ultrastructural level and these larvae would be in poor condition at settlement, reducing juvenile recruitment and overall survival. Elevated temperatures increased prodissoconch II sizes. However, the overall impacts on larval shell quality and integrity with concurrent ocean acidification would likely overshadow any beneficial results from warmer temperatures, limiting populations of this prevalent Antarctic species.

beta-diversity and species accumulation in antarctic coastal benthos: influence of habitat, distance and productivity on ecological connectivity.

High Antarctic coastal marine environments are comparatively pristine with strong environmental gradients, which make them important places to investigate biodiversity relationships. Defining how different environmental features contribute to shifts in beta-diversity is especially important as these shifts reflect both spatio-temporal variations in species richness and the degree of ecological separation between local and regional species pools. We used complementary techniques (species accumulation models, multivariate variance partitioning and generalized linear models) to assess how the roles of productivity, bio-physical habitat heterogeneity and connectivity change with spatial scales from metres to 100's of km. Our results demonstrated that the relative importance of specific processes influencing species accumulation and beta-diversity changed with increasing spatial scale, and that patterns were never driven by only one factor. Bio-physical habitat heterogeneity had a strong influence on beta-diversity at scales <290 km, while the effects of productivity were low and significant only at scales >40 km. Our analysis supports the emphasis on the analysis of diversity relationships across multiple spatial scales and highlights the unequal connectivity of individual sites to the regional species pool. This has important implications for resilience to habitat loss and community homogenisation, especially for Antarctic benthic communities where rates of recovery from disturbance are slow, there is a high ratio of poor-dispersing and brooding species, and high biogenic habitat heterogeneity and spatio-temporal variability in primary production make the system vulnerable to disturbance. Consequently, large areas need to be included within marine protected areas for effective management and conservation of these special ecosystems in the face of increasing anthropogenic disturbance.