Essential omega-3 fatty acids are depleted in sea ice and pelagic algae of the Central Arctic Ocean.

Microalgae are the main source of the omega-3 fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), essential for the healthy development of most marine and terrestrial fauna including humans. Inverse correlations of algal EPA and DHA proportions (% of total fatty acids) with temperature have led to suggestions of a warming-induced decline in the global production of these biomolecules and an enhanced importance of high latitude organisms for their provision. The cold Arctic Ocean is a potential hotspot of EPA and DHA production, but consequences of global warming are unknown. Here, we combine a full-seasonal EPA and DHA dataset from the Central Arctic Ocean (CAO), with results from 13 previous field studies and 32 cultured algal strains to examine five potential climate change effects; ice algae loss, community shifts, increase in light, nutrients, and temperature. The algal EPA and DHA proportions were lower in the ice-covered CAO than in warmer peripheral shelf seas, which indicates that the paradigm of an inverse correlation of EPA and DHA proportions with temperature may not hold in the Arctic. We found no systematic differences in the summed EPA and DHA proportions of sea ice versus pelagic algae, and in diatoms versus non-diatoms. Overall, the algal EPA and DHA proportions varied up to four-fold seasonally and 10-fold regionally, pointing to strong light and nutrient limitations in the CAO. Where these limitations ease in a warming Arctic, EPA and DHA proportions are likely to increase alongside increasing primary production, with nutritional benefits for a non-ice-associated food web.

Steeper size spectra with decreasing phytoplankton biomass indicate strong trophic amplification and future fish declines.

Under climate change, model ensembles suggest that declines in phytoplankton biomass amplify into greater reductions at higher trophic levels, with serious implications for fisheries and carbon storage. However, the extent and mechanisms of this trophic amplification vary greatly among models, and validation is problematic. In situ size spectra offer a novel alternative, comparing biomass of small and larger organisms to quantify the net efficiency of energy transfer through natural food webs that are already challenged with multiple climate change stressors. Our global compilation of pelagic size spectrum slopes supports trophic amplification empirically, independently from model simulations. Thus, even a modest (16%) decline in phytoplankton this century would magnify into a 38% decline in supportable biomass of fish within the intensively-fished mid-latitude ocean. We also show that this amplification stems not from thermal controls on consumers, but mainly from temperature or nutrient controls that structure the phytoplankton baseline of the food web. The lack of evidence for direct thermal effects on size structure contrasts with most current thinking, based often on more acute stress experiments or shorter-timescale responses. Our synthesis of size spectra integrates these short-term dynamics, revealing the net efficiency of food webs acclimating and adapting to climatic stressors.

Major declines in NE Atlantic plankton contrast with more stable populations in the rapidly warming North Sea.

Plankton form the base of marine food webs, making them important indicators of ecosystem status. Changes in the abundance of plankton functional groups, or lifeforms, can affect higher trophic levels and can indicate important shifts in ecosystem functioning. Here, we extend this knowledge by combining data from Continuous Plankton Recorder and fixed-point stations to provide the most comprehensive analysis of plankton time-series for the North-East Atlantic and North-West European shelf to date. We analysed 24 phytoplankton and zooplankton datasets from 15 research institutions to map 60-year abundance trends for 8 planktonic lifeforms. Most lifeforms decreased in abundance (e.g. dinoflagellates: -5 %, holoplankton: -7 % decade-1), except for meroplankton, which increased 12 % decade-1, reflecting widespread changes in large-scale and localised processes. K-means clustering of assessment units according to abundance trends revealed largely opposing trend direction between shelf and oceanic regions for most lifeforms, with North Sea areas characterised by increasing coastal abundance, while abundance decreased in North-East Atlantic areas. Individual taxa comprising each phytoplankton lifeform exhibited similar abundance trends, whereas taxa grouped within zooplankton lifeforms were more variable. These regional contrasts are counterintuitive, since the North Sea which has undergone major warming, changes in nutrients, and past fisheries perturbation has changed far less, from phytoplankton to fish larvae, as compared to the more slowly warming North-East Atlantic with lower nutrient supply and fishing pressure. This more remote oceanic region has shown a major and worrying decline in the traditional food web. Although the causal mechanisms remain unclear, declining abundance of key planktonic lifeforms in the North-East Atlantic, including diatoms and copepods, are a cause of major concern for the future of food webs and should provide a red flag to politicians and policymakers about the prioritisation of future management and adaptation measures required to ensure future sustainable use of the marine ecosystem.

Relationships of temperature and biodiversity with stability of natural aquatic food webs.

Temperature and biodiversity changes occur in concert, but their joint effects on ecological stability of natural food webs are unknown. Here, we assess these relationships in 19 planktonic food webs. We estimate stability as structural stability (using the volume contraction rate) and temporal stability (using the temporal variation of species abundances). Warmer temperatures were associated with lower structural and temporal stability, while biodiversity had no consistent effects on either stability property. While species richness was associated with lower structural stability and higher temporal stability, Simpson diversity was associated with higher temporal stability. The responses of structural stability were linked to disproportionate contributions from two trophic groups (predators and consumers), while the responses of temporal stability were linked both to synchrony of all species within the food web and distinctive contributions from three trophic groups (predators, consumers, and producers). Our results suggest that, in natural ecosystems, warmer temperatures can erode ecosystem stability, while biodiversity changes may not have consistent effects.

Monitoring and modelling marine zooplankton in a changing climate.

Zooplankton are major consumers of phytoplankton primary production in marine ecosystems. As such, they represent a critical link for energy and matter transfer between phytoplankton and bacterioplankton to higher trophic levels and play an important role in global biogeochemical cycles. In this Review, we discuss key responses of zooplankton to ocean warming, including shifts in phenology, range, and body size, and assess the implications to the biological carbon pump and interactions with higher trophic levels. Our synthesis highlights key knowledge gaps and geographic gaps in monitoring coverage that need to be urgently addressed. We also discuss an integrated sampling approach that combines traditional and novel techniques to improve zooplankton observation for the benefit of monitoring zooplankton populations and modelling future scenarios under global changes.

Stepping stones towards Antarctica: Switch to southern spawning grounds explains an abrupt range shift in krill.

Poleward range shifts are a global-scale response to warming, but these vary greatly among taxa and are hard to predict for individual species, localized regions or over shorter (years to decadal) timescales. Moving poleward might be easier in the Arctic than in the Southern Ocean, where evidence for range shifts is sparse and contradictory. Here, we compiled a database of larval Antarctic krill, Euphausia superba and, together with an adult database, it showed how their range shift is out of step with the pace of warming. During a 70-year period of rapid warming (1920s-1990s), distribution centres of both larvae and adults in the SW Atlantic sector remained fixed, despite warming by 0.5-1.0°C and losing sea ice. This was followed by a hiatus in surface warming and ice loss, yet during this period the distributions of krill life stages shifted greatly, by ~1000 km, to the south-west. Understanding the mechanism of such step changes is essential, since they herald system reorganizations that are hard to predict with current modelling approaches. We propose that the abrupt shift was driven by climatic controls acting on localized recruitment hotspots, superimposed on thermal niche conservatism. During the warming hiatus, the Southern Annular Mode index continued to become increasingly positive and, likely through reduced feeding success for larvae, this led to a precipitous decline in recruitment from the main reproduction hotspot along the southern Scotia Arc. This cut replenishment to the northern portion of the krill stock, as evidenced by declining density and swarm frequency. Concomitantly, a new, southern reproduction area developed after the 1990s, reinforcing the range shift despite the lack of surface warming. New spawning hotspots may provide the stepping stones needed for range shifts into polar regions, so planning of climate-ready marine protected areas should include these key areas of future habitat.

North Atlantic warming over six decades drives decreases in krill abundance with no associated range shift.

In the North Atlantic, euphausiids (krill) form a major link between primary production and predators including commercially exploited fish. This basin is warming very rapidly, with species expected to shift northwards following their thermal tolerances. Here we show, however, that there has been a 50% decline in surface krill abundance over the last 60 years that occurred in situ, with no associated range shift. While we relate these changes to the warming climate, our study is the first to document an in situ squeeze on living space within this system. The warmer isotherms are shifting measurably northwards but cooler isotherms have remained relatively static, stalled by the subpolar fronts in the NW Atlantic. Consequently the two temperatures defining the core of krill distribution (7-13 °C) were 8° of latitude apart 60 years ago but are presently only 4° apart. Over the 60 year period the core latitudinal distribution of euphausiids has remained relatively stable so a 'habitat squeeze', with loss of 4° of latitude in living space, could explain the decline in krill. This highlights that, as the temperature warms, not all species can track isotherms and shift northward at the same rate with both losers and winners emerging under the 'Atlantification' of the sub-Arctic.

Lowered cameras reveal hidden behaviors of Antarctic krill.

Antarctic krill (Euphausia superba, hereafter 'krill') exemplify the methodological challenges of studying small, mobile, aggregating pelagic organisms.1 Krill are a central species in the Southern Ocean food web, provide important biogeochemical functions and support a valuable commercial fishery.2 Most of what we know about krill has been derived from acoustic surveys and net samples, the former being essential for estimating krill biomass and catch limits. However, understanding krill behavior, particularly in the poorly-studied autumn-winter seasons, is key for management and conservation. Here, we used seasonal video observations collected with a profiling camera system of krill along the Western Antarctic Peninsula to reveal krill vertical distribution, aggregation density and individual behaviors that have remained hidden from traditional sampling methods.3.

Strengthening the evidence base for temperature-mediated phenological asynchrony and its impacts.

Climate warming has caused the seasonal timing of many components of ecological food chains to advance. In the context of trophic interactions, the match-mismatch hypothesis postulates that differential shifts can lead to phenological asynchrony with negative impacts for consumers. However, at present there has been no consistent analysis of the links between temperature change, phenological asynchrony and individual-to-population-level impacts across taxa, trophic levels and biomes at a global scale. Here, we propose five criteria that all need to be met to demonstrate that temperature-mediated trophic asynchrony poses a growing risk to consumers. We conduct a literature review of 109 papers studying 129 taxa, and find that all five criteria are assessed for only two taxa, with the majority of taxa only having one or two criteria assessed. Crucially, nearly every study was conducted in Europe or North America, and most studies were on terrestrial secondary consumers. We thus lack a robust evidence base from which to draw general conclusions about the risk that climate-mediated trophic asynchrony may pose to populations worldwide.

Increasing picocyanobacteria success in shelf waters contributes to long-term food web degradation.

Continental margins are disproportionally important for global primary production, fisheries and CO2 uptake. However, across the Northeast Atlantic shelves, there has been an ongoing summertime decline of key biota-large diatoms, dinoflagellates and copepods-that traditionally fuel higher tropic levels such as fish, sea birds and marine mammals. Here, we combine multiple time series with in situ process studies to link these declines to summer nutrient stress and increasing proportions of picophytoplankton that can comprise up to 90% of the combined pico- and nanophytoplankton biomass in coastal areas. Among the pico-fraction, it is the cyanobacterium Synechococcus that flourishes when iron and nitrogen resupply to surface waters are diminished. Our field data show how traits beyond small size give Synechococcus a competitive edge over pico- and nanoeukaryotes. Key is their ability to grow at low irradiances near the nutricline, which is aided by their superior light-harvesting system and high affinity to iron. However, minute size and lack of essential biomolecules (e.g. omega-3 polyunsaturated fatty acids and sterols) render Synechococcus poor primary producers to sustain shelf sea food webs efficiently. The combination of earlier spring blooms and lower summer food quantity and quality creates an increasing period of suboptimal feeding conditions for zooplankton at a time of year when their metabolic demand is highest. We suggest that this nutrition-related mismatch has contributed to the widespread, ~50% decline in summer copepod abundance we observe over the last 60 years. With Synechococcus clades being prominent from the tropics to the Arctic and their abundances increasing worldwide, our study informs projections of future food web dynamics in coastal and shelf areas where droughts and stratification lead to increasing nutrient starvation of surface waters.

Lifeform indicators reveal large-scale shifts in plankton across the North-West European shelf.

Increasing direct human pressures on the marine environment, coupled with climate-driven changes, is a concern to marine ecosystems globally. This requires the development and monitoring of ecosystem indicators for effective management and adaptation planning. Plankton lifeforms (broad functional groups) are sensitive indicators of marine environmental change and can provide a simplified view of plankton biodiversity, building an understanding of change in lower trophic levels. Here, we visualize regional-scale multi-decadal trends in six key plankton lifeforms as well as their correlative relationships with sea surface temperature (SST). For the first time, we collate trends across multiple disparate surveys, comparing the spatially and temporally extensive Continuous Plankton Recorder (CPR) survey (offshore) with multiple long-term fixed station-based time-series (inshore) from around the UK coastline. These analyses of plankton lifeforms showed profound long-term changes, which were coherent across large spatial scales. For example, 'diatom' and 'meroplankton' lifeforms showed strong alignment between surveys and coherent regional-scale trends, with the 1998-2017 decadal average abundance of meroplankton being 2.3 times that of 1958-1967 for CPR samples in the North Sea. This major, shelf-wide increase in meroplankton correlated with increasing SSTs, and contrasted with a general decrease in holoplankton (dominated by small copepods), indicating a changing balance of benthic and pelagic fauna. Likewise, inshore-offshore gradients in dinoflagellate trends, with contemporary increases inshore contrasting with multi-decadal decreases offshore (approx. 75% lower decadal mean abundance), urgently require the identification of causal mechanisms. Our lifeform approach allows the collation of many different data types and time-series across the NW European shelf, providing a crucial evidence base for informing ecosystem-based management, and the development of regional adaptation plans.

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.

Habitat partitioning in Antarctic krill: Spawning hotspots and nursery areas.

Antarctic krill, Euphausia superba, have a circumpolar distribution but are concentrated within the south-west Atlantic sector, where they support a unique food web and a commercial fishery. Within this sector, our first goal was to produce quantitative distribution maps of all six ontogenetic life stages of krill (eggs, nauplii plus metanauplii, calyptopes, furcilia, juveniles, and adults), based on a compilation of all available post 1970s data. Using these maps, we then examined firstly whether "hotspots" of egg production and early stage nursery occurred, and secondly whether the available habitat was partitioned between the successive life stages during the austral summer and autumn, when krill densities can be high. To address these questions, we compiled larval krill density records and extracted data spanning 41 years (1976-2016) from the existing KRILLBASE-abundance and KRILLBASE-length-frequency databases. Although adult males and females of spawning age were widely distributed, the distribution of eggs, nauplii and metanauplii indicates that spawning is most intense over the shelf and shelf slope. This contrasts with the distributions of calyptope and furcilia larvae, which were concentrated further offshore, mainly in the Southern Scotia Sea. Juveniles, however, were strongly concentrated over shelves along the Scotia Arc. Simple environmental analyses based on water depth and mean water temperature suggest that krill associate with different habitats over the course of their life cycle. From the early to late part of the austral season, juvenile distribution moves from ocean to shelf, opposite in direction to that for adults. Such habitat partitioning may reduce intraspecific competition for food, which has been suggested to occur when densities are exceptionally high during years of strong recruitment. It also prevents any potential cannibalism by adults on younger stages. Understanding the location of krill spawning and juvenile development in relation to potentially overlapping fishing activities is needed to protect the health of the south-west Atlantic sector ecosystem.

Zooplankton Gut Passage Mobilizes Lithogenic Iron for Ocean Productivity.

Iron is an essential nutrient for phytoplankton, but low concentrations limit primary production and associated atmospheric carbon drawdown in large parts of the world's oceans [1, 2]. Lithogenic particles deriving from aeolian dust deposition, glacial runoff, or river discharges can form an important source if the attached iron becomes dissolved and therefore bioavailable [3-5]. Acidic digestion by zooplankton is a potential mechanism for iron mobilization [6], but evidence is lacking. Here we show that Antarctic krill sampled near glacial outlets at the island of South Georgia (Southern Ocean) ingest large amounts of lithogenic particles and contain 3-fold higher iron concentrations in their muscle than specimens from offshore, which confirms mineral dissolution in their guts. About 90% of the lithogenic and biogenic iron ingested by krill is passed into their fecal pellets, which contain ∼5-fold higher proportions of labile (reactive) iron than intact diatoms. The mobilized iron can be released in dissolved form directly from krill or via multiple pathways involving microbes, other zooplankton, and krill predators. This can deliver substantial amounts of bioavailable iron and contribute to the fertilization of coastal waters and the ocean beyond. In line with our findings, phytoplankton blooms downstream of South Georgia are more intensive and longer lasting during years with high krill abundance on-shelf. Thus, krill crop phytoplankton but boost new production via their nutrient supply. Understanding and quantifying iron mobilization by zooplankton is essential to predict ocean productivity in a warming climate where lithogenic iron inputs from deserts, glaciers, and rivers are increasing [7-10].

Ocean net heat flux influences seasonal to interannual patterns of plankton abundance.

Changes in the net heat flux (NHF) into the ocean have profound impacts on global climate. We analyse a long-term plankton time-series and show that the NHF is a critical indicator of ecosystem dynamics. We show that phytoplankton abundance and diversity patterns are tightly bounded by the switches between negative and positive NHF over an annual cycle. Zooplankton increase before the transition to positive NHF in the spring but are constrained by the negative NHF switch in autumn. By contrast bacterial diversity is decoupled from either NHF switch, but is inversely correlated (r = -0.920) with the magnitude of the NHF. We show that the NHF is a robust mechanistic tool for predicting climate change indicators such as spring phytoplankton bloom timing and length of the growing season.

Sardine cycles, krill declines, and locust plagues: revisiting 'wasp-waist' food webs.

'Wasp-waist' systems are dominated by a mid trophic-level species that is thought to exert top-down control on its food and bottom-up control on its predators. Sardines, anchovy, and Antarctic krill are suggested examples, and here we use locusts to explore whether the wasp-waist concept also applies on land. These examples also display the traits of mobile aggregations and dietary diversity, which help to reduce the foraging footprint from their large, localised biomasses. This suggests that top-down control on their food operates at local aggregation scales and not at wider scales suggested by the original definition of wasp-waist. With this modification, the wasp-waist framework can cross-fertilise marine and terrestrial approaches, revealing how seemingly disparate but economically important systems operate.

Next generation sequencing reveals the hidden diversity of zooplankton assemblages.

BACKGROUND: Zooplankton play an important role in our oceans, in biogeochemical cycling and providing a food source for commercially important fish larvae. However, difficulties in correctly identifying zooplankton hinder our understanding of their roles in marine ecosystem functioning, and can prevent detection of long term changes in their community structure. The advent of massively parallel next generation sequencing technology allows DNA sequence data to be recovered directly from whole community samples. Here we assess the ability of such sequencing to quantify richness and diversity of a mixed zooplankton assemblage from a productive time series site in the Western English Channel. METHODOLOGY/PRINCIPLE FINDINGS: Plankton net hauls (200 µm) were taken at the Western Channel Observatory station L4 in September 2010 and January 2011. These samples were analysed by microscopy and metagenetic analysis of the 18S nuclear small subunit ribosomal RNA gene using the 454 pyrosequencing platform. Following quality control a total of 419,041 sequences were obtained for all samples. The sequences clustered into 205 operational taxonomic units using a 97% similarity cut-off. Allocation of taxonomy by comparison with the National Centre for Biotechnology Information database identified 135 OTUs to species level, 11 to genus level and 1 to order, <2.5% of sequences were classified as unknowns. By comparison a skilled microscopic analyst was able to routinely enumerate only 58 taxonomic groups. CONCLUSIONS: Metagenetics reveals a previously hidden taxonomic richness, especially for Copepoda and hard-to-identify meroplankton such as Bivalvia, Gastropoda and Polychaeta. It also reveals rare species and parasites. We conclude that Next Generation Sequencing of 18S amplicons is a powerful tool for elucidating the true diversity and species richness of zooplankton communities. While this approach allows for broad diversity assessments of plankton it may become increasingly attractive in future if sequence reference libraries of accurately identified individuals are better populated.

Potential climate change effects on the habitat of antarctic krill in the weddell quadrant of the southern ocean.

Antarctic krill is a cold water species, an increasingly important fishery resource and a major prey item for many fish, birds and mammals in the Southern Ocean. The fishery and the summer foraging sites of many of these predators are concentrated between 0° and 90°W. Parts of this quadrant have experienced recent localised sea surface warming of up to 0.2°C per decade, and projections suggest that further widespread warming of 0.27° to 1.08°C will occur by the late 21(st) century. We assessed the potential influence of this projected warming on Antarctic krill habitat with a statistical model that links growth to temperature and chlorophyll concentration. The results divide the quadrant into two zones: a band around the Antarctic Circumpolar Current in which habitat quality is particularly vulnerable to warming, and a southern area which is relatively insensitive. Our analysis suggests that the direct effects of warming could reduce the area of growth habitat by up to 20%. The reduction in growth habitat within the range of predators, such as Antarctic fur seals, that forage from breeding sites on South Georgia could be up to 55%, and the habitat's ability to support Antarctic krill biomass production within this range could be reduced by up to 68%. Sensitivity analysis suggests that the effects of a 50% change in summer chlorophyll concentration could be more significant than the direct effects of warming. A reduction in primary production could lead to further habitat degradation but, even if chlorophyll increased by 50%, projected warming would still cause some degradation of the habitat accessible to predators. While there is considerable uncertainty in these projections, they suggest that future climate change could have a significant negative effect on Antarctic krill growth habitat and, consequently, on Southern Ocean biodiversity and ecosystem services.

Long-term decline in krill stock and increase in salps within the Southern Ocean.

Antarctic krill (Euphausia superba) and salps (mainly Salpa thompsoni) are major grazers in the Southern Ocean, and krill support commercial fisheries. Their density distributions have been described in the period 1926-51, while recent localized studies suggest short-term changes. To examine spatial and temporal changes over larger scales, we have combined all available scientific net sampling data from 1926 to 2003. This database shows that the productive southwest Atlantic sector contains >50% of Southern Ocean krill stocks, but here their density has declined since the 1970s. Spatially, within their habitat, summer krill density correlates positively with chlorophyll concentrations. Temporally, within the southwest Atlantic, summer krill densities correlate positively with sea-ice extent the previous winter. Summer food and the extent of winter sea ice are thus key factors in the high krill densities observed in the southwest Atlantic Ocean. Krill need the summer phytoplankton blooms of this sector, where winters of extensive sea ice mean plentiful winter food from ice algae, promoting larval recruitment and replenishing the stock. Salps, by contrast, occupy the extensive lower-productivity regions of the Southern Ocean and tolerate warmer water than krill. As krill densities decreased last century, salps appear to have increased in the southern part of their range. These changes have had profound effects within the Southern Ocean food web.