Satellite sensor requirements for monitoring essential biodiversity variables of coastal ecosystems.

The biodiversity and high productivity of coastal terrestrial and aquatic habitats are the foundation for important benefits to human societies around the world. These globally distributed habitats need frequent and broad systematic assessments, but field surveys only cover a small fraction of these areas. Satellite-based sensors can repeatedly record the visible and near-infrared reflectance spectra that contain the absorption, scattering, and fluorescence signatures of functional phytoplankton groups, colored dissolved matter, and particulate matter near the surface ocean, and of biologically structured habitats (floating and emergent vegetation, benthic habitats like coral, seagrass, and algae). These measures can be incorporated into Essential Biodiversity Variables (EBVs), including the distribution, abundance, and traits of groups of species populations, and used to evaluate habitat fragmentation. However, current and planned satellites are not designed to observe the EBVs that change rapidly with extreme tides, salinity, temperatures, storms, pollution, or physical habitat destruction over scales relevant to human activity. Making these observations requires a new generation of satellite sensors able to sample with these combined characteristics: (1) spatial resolution on the order of 30 to 100-m pixels or smaller; (2) spectral resolution on the order of 5 nm in the visible and 10 nm in the short-wave infrared spectrum (or at least two or more bands at 1,030, 1,240, 1,630, 2,125, and/or 2,260 nm) for atmospheric correction and aquatic and vegetation assessments; (3) radiometric quality with signal to noise ratios (SNR) above 800 (relative to signal levels typical of the open ocean), 14-bit digitization, absolute radiometric calibration <2%, relative calibration of 0.2%, polarization sensitivity <1%, high radiometric stability and linearity, and operations designed to minimize sunglint; and (4) temporal resolution of hours to days. We refer to these combined specifications as H4 imaging. Enabling H4 imaging is vital for the conservation and management of global biodiversity and ecosystem services, including food provisioning and water security. An agile satellite in a 3-d repeat low-Earth orbit could sample 30-km swath images of several hundred coastal habitats daily. Nine H4 satellites would provide weekly coverage of global coastal zones. Such satellite constellations are now feasible and are used in various applications.

Tight coupling of primary production and marine mammal reproduction in the Southern Ocean.

Polynyas are areas of open water surrounded by sea ice and are important sources of primary production in high-latitude marine ecosystems. The magnitude of annual primary production in polynyas is controlled by the amount of exposure to solar radiation and sensitivity to changes in sea-ice extent. The degree of coupling between primary production and production by upper trophic-level consumers in these environments is not well understood, which prevents reliable predictions about population trajectories for species at higher trophic levels under potential future climate scenarios. In this study, we find a strong, positive relationship between annual primary production in an Antarctic polynya and pup production by ice-dependent Weddell seals. The timing of the relationship suggests reproductive effort increases to take advantage of high primary production occurring in the months after the birth pulse. Though the proximate causal mechanism is unknown, our results indicate tight coupling between organisms at disparate trophic levels on a short timescale, deepen our understanding of marine ecosystem processes, and raise interesting questions about why such coupling exists and what implications it has for understanding high-latitude ecosystems.

Massive difference in synonymous substitution rates among mitochondrial, plastid, and nuclear genes of Phaeocystis algae.

We are just beginning to understand how mutation rates differ among mitochondrial, plastid, and nuclear genomes. In most seed plants the mitochondrial mutation rate is estimated to be lower than those of the plastid and nucleus, whereas in the red alga Porphyra the opposite is true, and in certain green algae all three genomes appear to have similar rates of mutation. Relative rate statistics of organelle vs nuclear genes, however, are lacking for lineages that acquired their plastids through secondary endosymbiosis, but recent organelle DNA analyses suggest that they may differ drastically from what is observed in lineages with primary plastids, such as green plants and red algae. Here, by measuring synonymous nucleotide substitutions, we approximate the relative mutation rates within the haptophyte genus Phaeocystis, which has a red-algal-derived, secondary plastid. Synonymous-site divergence data indicate that for Phaeocystis antarctica and P. globosa the mitochondrial mutation rate is 10 and 3 times that of the plastid and nucleus, respectively. This differs drastically from relative rate estimates for primary-plastid-bearing lineages and presents a much more dynamic view of organelle vs nuclear mutation rates across the eukaryotic domain.

Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota.

Antarctic and Southern Ocean (ASO) marine ecosystems have been changing for at least the last 30 years, including in response to increasing ocean temperatures and changes in the extent and seasonality of sea ice; the magnitude and direction of these changes differ between regions around Antarctica that could see populations of the same species changing differently in different regions. This article reviews current and expected changes in ASO physical habitats in response to climate change. It then reviews how these changes may impact the autecology of marine biota of this polar region: microbes, zooplankton, salps, Antarctic krill, fish, cephalopods, marine mammals, seabirds, and benthos. The general prognosis for ASO marine habitats is for an overall warming and freshening, strengthening of westerly winds, with a potential pole-ward movement of those winds and the frontal systems, and an increase in ocean eddy activity. Many habitat parameters will have regionally specific changes, particularly relating to sea ice characteristics and seasonal dynamics. Lower trophic levels are expected to move south as the ocean conditions in which they are currently found move pole-ward. For Antarctic krill and finfish, the latitudinal breadth of their range will depend on their tolerance of warming oceans and changes to productivity. Ocean acidification is a concern not only for calcifying organisms but also for crustaceans such as Antarctic krill; it is also likely to be the most important change in benthic habitats over the coming century. For marine mammals and birds, the expected changes primarily relate to their flexibility in moving to alternative locations for food and the energetic cost of longer or more complex foraging trips for those that are bound to breeding colonies. Few species are sufficiently well studied to make comprehensive species-specific vulnerability assessments possible. Priorities for future work are discussed.

Seasonal Water Mass Evolution and Non-Redfield Dynamics Enhance CO2 Uptake in the Chukchi Sea.

The Chukchi Sea is an increasing CO2 sink driven by rapid climate changes. Understanding the seasonal variation of air-sea CO2 exchange and the underlying mechanisms of biogeochemical dynamics is important for predicting impacts of climate change on and feedbacks by the ocean. Here, we present a unique data set of underway sea surface partial pressure of CO2 (pCO2) and discrete samples of biogeochemical properties collected in five consecutive cruises in 2014 and examine the seasonal variations in air-sea CO2 flux and net community production (NCP). We found that thermal and non-thermal effects have different impacts on sea surface pCO2 and thus the air-sea CO2 flux in different water masses. The Bering summer water combined with meltwater has a significantly greater atmospheric CO2 uptake potential than that of the Alaskan Coastal Water in the southern Chukchi Sea in summer, due to stronger biological CO2 removal and a weaker thermal effect. By analyzing the seasonal drawdown of dissolved inorganic carbon (DIC) and nutrients, we found that DIC-based NCP was higher than nitrate-based NCP by 66%-84% and attributable to partially decoupled C and N uptake because of a variable phytoplankton stoichiometry. A box model with a non-Redfield C:N uptake ratio can adequately reproduce observed pCO2 and DIC, which reveals that, during the intensive growing season (late spring to early summer), 30%-46% CO2 uptake in the Chukchi Sea was supported by a flexible stoichiometry of phytoplankton. These findings have important ramification for forecasting the responses of CO2 uptake of the Chukchi ecosystem to climate change.

Marine microorganisms and global nutrient cycles.

The way that nutrients cycle through atmospheric, terrestrial, oceanic and associated biotic reservoirs can constrain rates of biological production and help structure ecosystems on land and in the sea. On a global scale, cycling of nutrients also affects the concentration of atmospheric carbon dioxide. Because of their capacity for rapid growth, marine microorganisms are a major component of global nutrient cycles. Understanding what controls their distributions and their diverse suite of nutrient transformations is a major challenge facing contemporary biological oceanographers. What is emerging is an appreciation of the previously unknown degree of complexity within the marine microbial community.

Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean.

Biological productivity in most of the world's oceans is controlled by the supply of nutrients to surface waters. The relative balance between supply and removal of nutrients--including nitrogen, iron and phosphorus--determines which nutrient limits phytoplankton growth. Although nitrogen limits productivity in much of the ocean, large portions of the tropics and subtropics are defined by extreme nitrogen depletion. In these regions, microbial denitrification removes biologically available forms of nitrogen from the water column, producing substantial deficits relative to other nutrients. Here we demonstrate that nitrogen-deficient areas of the tropical and subtropical oceans are acutely vulnerable to nitrogen pollution. Despite naturally high nutrient concentrations and productivity, nitrogen-rich agricultural runoff fuels large (54-577 km2) phytoplankton blooms in the Gulf of California. Runoff exerts a strong and consistent influence on biological processes, in 80% of cases stimulating blooms within days of fertilization and irrigation of agricultural fields. We project that by the year 2050, 27-59% of all nitrogen fertilizer will be applied in developing regions located upstream of nitrogen-deficient marine ecosystems. Our findings highlight the present and future vulnerability of these ecosystems to agricultural runoff.

UCYN-A/haptophyte symbioses dominate N2 fixation in the Southern California Current System.

The availability of fixed nitrogen (N) is an important factor limiting biological productivity in the oceans. In coastal waters, high dissolved inorganic N concentrations were historically thought to inhibit dinitrogen (N2) fixation, however, recent N2 fixation measurements and the presence of the N2-fixing UCYN-A/haptophyte symbiosis in nearshore waters challenge this paradigm. We characterized the contribution of UCYN-A symbioses to nearshore N2 fixation in the Southern California Current System (SCCS) by measuring bulk community and single-cell N2 fixation rates, as well as diazotroph community composition and abundance. UCYN-A1 and UCYN-A2 symbioses dominated diazotroph communities throughout the region during upwelling and oceanic seasons. Bulk N2 fixation was detected in most surface samples, with rates up to 23.0 ± 3.8 nmol N l-1 d-1, and was often detected at the deep chlorophyll maximum in the presence of nitrate (>1 µM). UCYN-A2 symbiosis N2 fixation rates were higher (151.1 ± 112.7 fmol N cell-1 d-1) than the UCYN-A1 symbiosis (6.6 ± 8.8 fmol N cell-1 d-1). N2 fixation by the UCYN-A1 symbiosis accounted for a majority of the measured bulk rates at two offshore stations, while the UCYN-A2 symbiosis was an important contributor in three nearshore stations. This report of active UCYN-A symbioses and broad mesoscale distribution patterns establishes UCYN-A symbioses as the dominant diazotrophs in the SCCS, where heterocyst-forming and unicellular cyanobacteria are less prevalent, and provides evidence that the two dominant UCYN-A sublineages are separate ecotypes.

Massive Southern Ocean phytoplankton bloom fed by iron of possible hydrothermal origin.

Primary production in the Southern Ocean (SO) is limited by iron availability. Hydrothermal vents have been identified as a potentially important source of iron to SO surface waters. Here we identify a recurring phytoplankton bloom in the high-nutrient, low-chlorophyll waters of the Antarctic Circumpolar Current in the Pacific sector of the SO, that we argue is fed by iron of hydrothermal origin. In January 2014 the bloom covered an area of ~266,000 km2 with depth-integrated chlorophyll a > 300 mg m-2, primary production rates >1 g C m-2 d-1, and a mean CO2 flux of -0.38 g C m-2 d-1. The elevated iron supporting this bloom is likely of hydrothermal origin based on the recurrent position of the bloom relative to two active hydrothermal vent fields along the Australian Antarctic Ridge and the association of the elevated iron with a distinct water mass characteristic of a nonbuoyant hydrothermal vent plume.

Responding to climate change: Adélie Penguins confront astronomical and ocean boundaries.

Long-distance migration enables many organisms to take advantage of lucrative breeding and feeding opportunities during summer at high latitudes and then to move to lower, more temperate latitudes for the remainder of the year. The latitudinal range of the Adélie Penguin (Pygoscelis adeliae) spans approximately 22 degrees. Penguins from northern colonies may not migrate, but due to the high latitude of Ross Island colonies, these penguins almost certainly undertake the longest migrations for the species. Previous work has suggested that Adélies require both pack ice and some ambient light at all times of year. Over a three-year period, which included winters of both extensive and reduced sea ice, we investigated characteristics of migratory routes and wintering locations of Adélie Penguins from two colonies of very different size on Ross Island, Ross Sea, the southernmost colonies for any penguin. We acquired data from 3-16 geolocation sensor tags (GLS) affixed to penguins each year at both Cape Royds and Cape Crozier in 2003-2005. Migrations averaged 12760 km, with the longest being 17 600 km, and were in part facilitated by pack ice movement. Trip distances varied annually, but not by colony. Penguins rarely traveled north of the main sea-ice pack, and used areas with high sea-ice concentration, ranging from 75% to 85%, about 500 km inward from the ice edge. They also used locations where there was some twilight (2-7 h with sun < 6 degrees below the horizon). We report the present Adélie Penguin migration pattern and conjecture on how it probably has changed over the past approximately 12000 years, as the West Antarctic Ice Sheet withdrew southward across the Ross Sea, a situation that no other Adélie Penguin population has had to confront. As sea ice extent in the Ross Sea sector decreases in the near future, as predicted by climate models, we can expect further changes in the migration patterns of the Ross Sea penguins.

Unusual marine cyanobacteria/haptophyte symbiosis relies on N2 fixation even in N-rich environments.

The microbial fixation of N2 is the largest source of biologically available nitrogen (N) to the oceans. However, it is the most energetically expensive N-acquisition process and is believed inhibited when less energetically expensive forms, like dissolved inorganic N (DIN), are available. Curiously, the cosmopolitan N2-fixing UCYN-A/haptophyte symbiosis grows in DIN-replete waters, but the sensitivity of their N2 fixation to DIN is unknown. We used stable isotope incubations, catalyzed reporter deposition fluorescence in-situ hybridization (CARD-FISH), and nanoscale secondary ion mass spectrometry (nanoSIMS), to investigate the N source used by the haptophyte host and sensitivity of UCYN-A N2 fixation in DIN-replete waters. We demonstrate that under our experimental conditions, the haptophyte hosts of two UCYN-A sublineages do not assimilate nitrate (NO3-) and meet little of their N demands via ammonium (NH4+) uptake. Instead the UCYN-A/haptophyte symbiosis relies on UCYN-A N2 fixation to supply large portions of the haptophyte's N requirements, even under DIN-replete conditions. Furthermore, UCYN-A N2 fixation rates, and haptophyte host carbon fixation rates, were at times stimulated by NO3- additions in N-limited waters suggesting a link between the activities of the bulk phytoplankton assemblage and the UCYN-A/haptophyte symbiosis. The results suggest N2 fixation may be an evolutionarily viable strategy for diazotroph-eukaryote symbioses, even in N-rich coastal or high latitude waters.

Zooplankton and micronekton respond to climate fluctuations in the Amundsen Sea polynya, Antarctica.

The vertical migration of zooplankton and micronekton (hereafter 'zooplankton') has ramifications throughout the food web. Here, we present the first evidence that climate fluctuations affect the vertical migration of zooplankton in the Southern Ocean, based on multi-year acoustic backscatter data from one of the deep troughs in the Amundsen Sea, Antarctica. High net primary productivity (NPP) and the annual variation in seasonal ice cover make the Amundsen Sea coastal polynya an ideal site in which to examine how zooplankton behavior responds to climate fluctuations. Our observations show that the timing of the seasonal vertical migration and abundance of zooplankton in the seasonally varying sea ice is correlated with the Southern Annular Mode (SAM) and El Niño Southern Oscillation (ENSO). Zooplankton in this region migrate seasonally and overwinter at depth, returning to the surface in spring. During +SAM/La Niña periods, the at-depth overwintering period is shorter compared to -SAM/El Niño periods, and return to the surface layers starts earlier in the year. These differences may result from the higher sea ice cover and decreased NPP during +SAM/La Niña periods. This observation points to a new link between global climate fluctuations and the polar marine food web.

Sea ice ecosystems.

Polar sea ice is one of the largest ecosystems on Earth. The liquid brine fraction of the ice matrix is home to a diverse array of organisms, ranging from tiny archaea to larger fish and invertebrates. These organisms can tolerate high brine salinity and low temperature but do best when conditions are milder. Thriving ice algal communities, generally dominated by diatoms, live at the ice/water interface and in recently flooded surface and interior layers, especially during spring, when temperatures begin to rise. Although protists dominate the sea ice biomass, heterotrophic bacteria are also abundant. The sea ice ecosystem provides food for a host of animals, with crustaceans being the most conspicuous. Uneaten organic matter from the ice sinks through the water column and feeds benthic ecosystems. As sea ice extent declines, ice algae likely contribute a shrinking fraction of the total amount of organic matter produced in polar waters.

The oceanography and ecology of the Ross Sea.

The continental shelf of the Ross Sea exhibits substantial variations in physical forcing, ice cover, and biological processes on a variety of time and space scales. Its circulation is characterized by advective inputs from the east and exchanges with off-shelf regions via the troughs along the northern portions. Phytoplankton biomass is greater there than anywhere else in the Antarctic, although nitrate is rarely reduced to levels below 10 µmol L(-1). Overall growth is regulated by irradiance (via ice at the surface and by the depths of the mixed layers) and iron concentrations. Apex predators reach exceptional abundances, and the world's largest colonies of Adélie and emperor penguins are found there. Krill are represented by two species (Euphausia superba near the shelf break and Euphausia crystallorophias throughout the continental shelf region). Equally important and poorly known is the Antarctic silverfish (Pleuragramma antarcticum), which is also consumed by most upper-trophic-level predators. Future changes in the Ross Sea environment will have profound and unpredictable effects on the food web.

Productivity in the barents sea--response to recent climate variability.

The temporal and spatial dynamics of primary and secondary biomass/production in the Barents Sea since the late 1990s are examined using remote sensing data, observations and a coupled physical-biological model. Field observations of mesozooplankton biomass, and chlorophyll a data from transects (different seasons) and large-scale surveys (autumn) were used for validation of the remote sensing products and modeling results. The validation showed that satellite data are well suited to study temporal and spatial dynamics of chlorophyll a in the Barents Sea and that the model is an essential tool for secondary production estimates. Temperature, open water area, chlorophyll a, and zooplankton biomass show large interannual variations in the Barents Sea. The climatic variability is strongest in the northern and eastern parts. The moderate increase in net primary production evident in this study is likely an ecosystem response to changes in climate during the same period. Increased open water area and duration of open water season, which are related to elevated temperatures, appear to be the key drivers of the changes in annual net primary production that has occurred in the northern and eastern areas of this ecosystem. The temporal and spatial variability in zooplankton biomass appears to be controlled largely by predation pressure. In the southeastern Barents Sea, statistically significant linkages were observed between chlorophyll a and zooplankton biomass, as well as between net primary production and fish biomass, indicating bottom-up trophic interactions in this region.

THE EFFECT OF IRON LIMITATION ON THE PHOTOPHYSIOLOGY OF PHAEOCYSTIS ANTARCTICA (PRYMNESIOPHYCEAE) AND FRAGILARIOPSIS CYLINDRUS (BACILLARIOPHYCEAE) UNDER DYNAMIC IRRADIANCE(1).

The effects of iron limitation on photoacclimation to dynamic irradiance were studied in Phaeocystis antarctica G. Karst. and Fragilariopsis cylindrus (Grunow) W. Krieg. in terms of growth rate, photosynthetic parameters, pigment composition, and fluorescence characteristics. Under dynamic light conditions mimicking vertical mixing below the euphotic zone, P. antarctica displayed higher growth rates than F. cylindrus both under iron (Fe)-replete and Fe-limiting conditions. Both species showed xanthophyll de-epoxidation that was accompanied by low levels of nonphotochemical quenching (NPQ) during the irradiance maximum of the light cycle. The potential for NPQ at light levels corresponding to full sunlight was substantial in both species and increased under Fe limitation in F. cylindrus. Although the decline in Fv /Fm under Fe limitation was similar in both species, the accompanying decrease in the maximum rate of photosynthesis and growth rate was much stronger in F. cylindrus. Analysis of the electron transport rates through PSII and on to carbon (C) fixation revealed a large potential for photoprotective cyclic electron transport (CET) in F. cylindrus, particularly under Fe limitation. Probably, CET aided the photoprotection in F. cylindrus, but it also reduced photosynthetic efficiency at higher light intensities. P. antarctica, on the other hand, was able to efficiently use electrons flowing through PSII for C fixation at all light levels, particularly under Fe limitation. Thus, Fe limitation enhanced the photophysiological differences between P. antarctica and diatoms, supporting field observations where P. antarctica is found to dominate deeply mixed water columns, whereas diatoms dominate shallower mixed layers.

Massive phytoplankton blooms under Arctic sea ice.

Phytoplankton blooms over Arctic Ocean continental shelves are thought to be restricted to waters free of sea ice. Here, we document a massive phytoplankton bloom beneath fully consolidated pack ice far from the ice edge in the Chukchi Sea, where light transmission has increased in recent decades because of thinning ice cover and proliferation of melt ponds. The bloom was characterized by high diatom biomass and rates of growth and primary production. Evidence suggests that under-ice phytoplankton blooms may be more widespread over nutrient-rich Arctic continental shelves and that satellite-based estimates of annual primary production in these waters may be underestimated by up to 10-fold.

Photophysiology in two major southern ocean phytoplankton taxa: photosynthesis and growth of Phaeocystis antarctica and Fragilariopsis cylindrus under different irradiance levels.

The Ross Sea, Antarctica, supports two distinct populations of phytoplankton, one that grows well in sea ice and blooms in the shallow mixed layers of the Western marginal ice zone and the other that can be found in sea ice but thrives in the deeply mixed layers of the Ross Sea. Dominated by diatoms (e.g. Fragilariopsis cylindrus) and the prymnesiophyte Phaeocystis antarctica, respectively, the processes leading to the development of these different phytoplankton assemblages are not well known. The goal of this article was to gain a better understanding of the photophysiological characteristics that allow each taxon to dominate its specific habitat. Cultures of F. cylindrus and P. antarctica were each grown semi-continuously at four different constant irradiances (5, 25, 65, and 125 µmol quanta/m2/s). Fragilariopsis cylindrus produced far less photosynthetic pigment per cell than did P. antarctica but much more photoprotective pigment. Fragilariopsis cylindrus also exhibited substantially lower rates of photosynthesis and growth but also was far less susceptible to photoinhibition of cell growth. Excess photosynthetic capacity, a measure of the ability of phytoplankton to exploit variable light environments, was significantly higher in both strains of P. antarctica than in F. cylindrus. The combination of these characteristics suggests that F. cylindrus has a competitive advantage under conditions where mixed layers are shallow and light levels are relatively constant and high. In contrast, P. antarctica should dominate waters where mixed layers are deep and light levels are variable. These results are consistent with distributions of phytoplankton in the Ross Sea and suggest that light is the primary factor determining composition of phytoplankton communities.

UNDERSTANDING NITROGEN LIMITATION IN AUREOCOCCUS ANOPHAGEFFERENS (PELAGOPHYCEAE) THROUGH cDNA AND qRT-PCR ANALYSIS(1).

Brown tides of the marine pelagophyte Aureococcus anophagefferens Hargraves et Sieburth have been investigated extensively for the past two decades. Its growth is fueled by a variety of nitrogen (N) compounds, with dissolved organic nitrogen (DON) being particularly important during blooms. Characterization of a cDNA library suggests that A. anophagefferens can assimilate eight different forms of N. Expression of genes related to the sensing, uptake, and assimilation of inorganic and organic N, as well as the catabolic process of autophagy, was assayed in cells grown on different N sources and in N-limited cells. Growth on nitrate elicited an increase in the relative expression of nitrate and ammonium transporters, a nutrient stress-induced transporter, and a sensory kinase. Growth on urea increased the relative expression of a urea and a formate/nitrite transporter, while growth on ammonium resulted in an increase in the relative expression of an ammonium transporter, a novel ATP-binding cassette (ABC) transporter and a putative high-affinity phosphate transporter. N limitation resulted in a 30- to 110-fold increase in the relative expression of nitrate, ammonium, urea, amino acid/polyamine, and formate/nitrite transporters. A. anophagefferens demonstrated the highest relative accumulation of a transcript encoding a novel purine transporter, which was highly expressed across all N sources. This finding suggests that purines are an important source of N for the growth of this organism and could possibly contribute to the initiation and maintenance of blooms in the natural environment.