Temporal and spatial trends in marine carbon isotopes in the Arctic Ocean and implications for food web studies

The Arctic is undergoing unprecedented environmental change. Rapid warming, decline in sea ice extent, increase in riverine input, ocean acidification and changes in primary productivity are creating a crucible for multiple concurrent environmental stressors, with unknown consequences for the entire arctic ecosystem. Here, we synthesized 30 years of data on the stable carbon isotope (δ¹³C) signatures in dissolved inorganic carbon (δ¹³C‐DIC; 1977–2014), marine and riverine particulate organic carbon (δ¹³C‐POC; 1986–2013) and tissues of marine mammals in the Arctic. δ¹³C values in consumers can change as a result of environmentally driven variation in the δ¹³C values at the base of the food web or alteration in the trophic structure, thus providing a method to assess the sensitivity of food webs to environmental change. Our synthesis reveals a spatially heterogeneous and temporally evolving δ¹³C baseline, with spatial gradients in the δ¹³C‐POC values between arctic shelves and arctic basins likely driven by differences in productivity and riverine and coastal influence. We report a decline in δ¹³C‐DIC values (?0.011‰ per year) in the Arctic, reflecting increasing anthropogenic carbon dioxide (CO₂) in the Arctic Ocean (i.e. Suess effect), which is larger than predicted. The larger decline in δ¹³C‐POC values and δ¹³C in arctic marine mammals reflects the anthropogenic CO₂ signal as well as the influence of a changing arctic environment. Combining the influence of changing sea ice conditions and isotopic fractionation by phytoplankton, we explain the decadal decline in δ¹³C‐POC values in the Arctic Ocean and partially explain the δ¹³C values in marine mammals with consideration of time‐varying integration of δ¹³C values. The response of the arctic ecosystem to ongoing environmental change is stronger than we would predict theoretically, which has tremendous implications for the study of food webs in the rapidly changing Arctic Ocean.     

A novel spatio-temporal scale based on ocean currents unravels environmental drivers of reproductive timing in a marine predator

Life-history strategies have evolved in response to predictable patterns of environmental features. In practice, linking life-history strategies and changes in environmental conditions requires comparable space–time scales between both processes, a difficult match in most marine system studies. We propose a novel spatio-temporal and dynamic scale to explore marine productivity patterns probably driving reproductive timing in the inshore little penguin (Eudyptula minor), based on monthly data on ocean circulation in the Southern Ocean, Australia. In contrast to what occurred when considering any other fixed scales, little penguin''s highly variable laying date always occurred within the annual peak of ocean productivity that emerged from our newly defined dynamic scale. Additionally, local sea surface temperature seems to have triggered the onset of reproduction, acting as an environmental cue informing on marine productivity patterns at our dynamic scale. Chlorophyll-a patterns extracted from this scale revealed that environment factors in marine ecosystems affecting breeding decisions are related to a much wider region than foraging areas that are commonly used in current studies investigating the link between animals'' life history and their environment. We suggest that marine productivity patterns may be more predictable than previously thought when environmental and biological data are examined at appropriate scales.     

Macromolecular production of phytoplankton in the northern Bering Sea, 2007

Photosynthetic carbon allocations into different macromolecular classes provide important clues regarding physiological conditions of phytoplankton and the nutritional status of potential grazers. The productivity experiments for photosynthetic carbon allocations were conducted at three light depths (100, 30, and 1 %) for nine different stations in the northern Bering Sea as an important gateway into the western Arctic Ocean, using the ¹³C isotope tracer technique to determine the major controlling factors and physiological conditions of phytoplankton. The photosynthetic carbon allocations into different macromolecular classes [Low molecular weight metabolites (LMWM), lipids, proteins, and polysaccharides] of primary producers were determined based on the productivity experiments. LMWM and polysaccharides had similar vertical patterns whereas lipids and proteins had reverse vertical patterns at all the stations, which is consistent with other results under different light depths. The overall average allocations were 37.9 (SD = ± 18.8 %), 26.6 (SD = ± 17.4 %), 26.5 (SD = ± 20.7 %), and 9.1 % (SD = ± 7.8 %), for LMWM, lipids, proteins, and polysaccharides, respectively. Based on a general pattern of macromolecular production in the northern Bering Sea, phytoplankton was in a physiologically transitional phase from an unlimited status to a nitrogen-deficient condition during our cruise period, 2007. However, more in situ field measurements for macromolecular production under a variety of environmental conditions will improve the understanding of the physiological responses of phytoplankton to the ongoing environmental changes in the Arctic Ocean.     

Marine biological controls on climate via the carbon and sulphur geochemical cycles

We review aspects of the influence of the marine biota on climate, focusing particularly on their role in mediating surface temperatures via their influence on atmospheric carbon dioxide (CO₂) and dimethyl sulphide (DMS) concentrations. Variation in natural CO₂ concentrations occurring over 10³ to 10⁵ years are set by oceanic processes, and in particular by conditions in the Southern Ocean, so it is to this region that we must look to understand the glacial-interglacial changes in CO₂ concentrations. It seems likely that marine productivity in the Southern Ocean is limited by a combination of restricted iron supply to the region and insufficient light. Plankton-produced DMS is thought to influence climate by changing the numbers of cloud condensation nuclei available in remote regions; the efficiency of this mechanism is still unknown, but calculations suggest it may be a powerful influence on climate. It has a much shorter time-scale than the CO₂ effect, and as a consequence may well be a player on the ''global change'' timescale. The direction of both the CO₂ and the DMS mechanisms is such that more marine productivity would lead to lower global temperatures, and we speculate that the overall effect of the marine biota today is to cool the planet by ca. 6°C as a result of these two mechanisms, with one-third of this figure being due to CO₂ effects and two-thirds due to DMS. While the marine biota influence climate, climate also influences the marine biota, chiefly via changing atmospheric circulation. This in turn alters ocean circulation patterns, responsible for mixing up sub-surface nutrients, and also influences the transport of nutrients, such as iron, in atmospheric dust. A more vigorous atmospheric circulation would be expected to increase the productivity of the marine biota on both counts. Thus during glacial time, the colder and drier climate might be expected to stimulate greater marine productivity than occurs today. Since more production leads to greater cooling by reduction in CO₂ and increase in DMS, the marine biota-climate system appears to have been in positive feedback in the glacial-interglacial transition, with the changes in the climate system being reinforced by changes in the marine biota. In the context of anthropogenic change, we cannot at present say what sign the feedback on climate will have, because we have no clear idea whether circulation will become more or less vigorous in the future.     

Trends in tuna carbon isotopes suggest global changes in pelagic phytoplankton communities

Considerable uncertainty remains over how increasing atmospheric CO₂ and anthropogenic climate changes are affecting open‐ocean marine ecosystems from phytoplankton to top predators. Biological time series data are thus urgently needed for the world's oceans. Here, we use the carbon stable isotope composition of tuna to provide a first insight into the existence of global trends in complex ecosystem dynamics and changes in the oceanic carbon cycle. From 2000 to 2015, considerable declines in δ¹³C values of 0.8‰–2.5‰ were observed across three tuna species sampled globally, with more substantial changes in the Pacific Ocean compared to the Atlantic and Indian Oceans. Tuna recorded not only the Suess effect, that is, fossil fuel‐derived and isotopically light carbon being incorporated into marine ecosystems, but also recorded profound changes at the base of marine food webs. We suggest a global shift in phytoplankton community structure, for example, a reduction in ¹³C‐rich phytoplankton such as diatoms, and/or a change in phytoplankton physiology during this period, although this does not rule out other concomitant changes at higher levels in the food webs. Our study establishes tuna δ¹³C values as a candidate essential ocean variable to assess complex ecosystem responses to climate change at regional to global scales and over decadal timescales. Finally, this time series will be invaluable in calibrating and validating global earth system models to project changes in marine biota.     

An empirical model of carbon flow through marine viruses and microzooplankton grazers

Viruses and microzooplankton grazers represent major sources of mortality for marine phytoplankton and bacteria, redirecting the flow of organic material throughout the world's oceans. Here, we investigate the use of nonlinear population models of interactions between phytoplankton, viruses and grazers as a means to quantitatively constrain the flow of carbon through marine microbial ecosystems. We augment population models with a synthesis of laboratory-based estimates of prey, predator and viral life history traits that constrain transfer efficiencies. We then apply the model framework to estimate loss rates in the California Current Ecosystem (CCE). With our empirically parameterized model, we estimate that, of the total losses mediated by viruses and microzooplankton grazing at the focal CCE site, 22 ± 3%, 46 ± 27%, 3 ± 2% and 29 ± 20% were directed to grazers, sloppy feeding (as well as excretion and respiration), viruses and viral lysate respectively. We identify opportunities to leverage ecosystem models and conventional mortality assays to further constrain the quantitative rates of critical ecosystem processes.     

Marine biodiversification in response to evolving phytoplankton stoichiometry

Diversification of the marine biosphere is intimately linked to the evolution of the biogeochemical cycles of carbon, nutrients, and primary productivity. A meta-analysis of the ratio of carbon-to-phosphorus buried in sedimentary rocks during the past 3 billion years indicates that both food quantity and, critically, food quality increased through time as a result of the evolving stoichiometry (nutrient content) of eukaryotic phytoplankton. Evolving food quantity and quality was primarily a function of broad tectonic cycles that influenced not just carbon burial, but also nutrient availability and primary productivity. Increasing nutrient availability during the middle-to-Late Proterozoic culminated in the production of food (phytoplankton biomass and fresh dead organic matter) with C:P Redfield ratios sufficient to finally promote geologically-rapid biodiversification during the Proterozoic–Phanerozoic transition. This resulted in further, massive nutrient sequestration into biomass that triggered positive feedback via nutrient recycling (bioturbation, mesozooplankton grazing) on phytoplankton productivity. Increasing rates and depths of bioturbation through the Phanerozoic suggest that nutrient recycling continued to increase. Increasing bioturbation and nutrient cycling appear to have been necessary to sustain the primary productivity and “energetics” (biomass, metabolic rates, and physical activity such as predation) of the marine biosphere because of the geologically-slow input of macronutrients like phosphorus from land and the continued sequestration of nutrients into marine and terrestrial biomass.     

Individual and interactive effects of ocean acidification,global warming,and UV radiation on phytoplankton

Rising carbon dioxide (CO₂) concentrations in the atmosphere result in increasing global temperatures and ocean warming (OW). Concomitantly, dissolution of anthropogenic CO₂ declines seawater pH, resulting in ocean acidification (OA) and altering marine chemical environments. The marine biological carbon pump driven by marine photosynthesis plays an important role for oceanic carbon sinks. Therefore, how ocean climate changes affect the amount of carbon fixation by primary producers is closely related to future ocean carbon uptake. OA may upregulate metabolic pathways in phytoplankton, such as upregulating ß-oxidation and the tricarboxylic acid cycle, resulting in increased accumulation of toxic phenolic compounds. Ocean warming decreases global phytoplankton productivity; however, regionally, it may stimulate primary productivity and change phytoplankton community composition, due to different physical and chemical environmental requirements of species. It is still controversial how OA and OW interactively affect marine carbon fixation by photosynthetic organisms. OA impairs the process of calcification in calcifying phytoplankton and aggravate ultraviolet (UV)-induced harms to the cells. Increasing temperatures enhance the activity of cellular repair mechanisms, which mitigates UV-induced damage. The effects of OA, warming, enhanced exposure to UV-B as well as the interactions of these environmental stress factors on phytoplankton productivity and community composition, are discussed in this review.     

Viral lysis modifies seasonal phytoplankton dynamics and carbon flow in the Southern Ocean

Phytoplankton form the base of marine food webs and are a primary means for carbon export in the Southern Ocean, a key area for global pCO₂ drawdown. Viral lysis and grazing have very different effects on microbial community dynamics and carbon export, yet, very little is known about the relative magnitude and ecological impact of viral lysis on natural phytoplankton communities, especially in Antarctic waters. Here, we report on the temporal dynamics and relative importance of viral lysis rates, in comparison to grazing, for Antarctic nano- and pico-sized phytoplankton of varied taxonomy and size over a full productive season. Our results show that viral lysis was a major loss factor throughout the season, responsible for roughly half (58%) of seasonal phytoplankton carbon losses. Viral lysis appeared critically important for explaining temporal dynamics and for obtaining a complete seasonal mass balance of Antarctic phytoplankton. Group-specific responses indicated a negative correlation between grazing and viral losses in Phaeocystis and picoeukaryotes, while for other phytoplankton groups losses were more evenly spread throughout the season. Cryptophyte mortality was dominated by viral lysis, whereas small diatoms were mostly grazed. Larger diatoms dominated algal carbon flow and a single ‘lysis event’ directed >100% of daily carbon production away from higher trophic levels. This study highlights the need to consider viral lysis of key Antarctic phytoplankton for a better understanding of microbial community interactions and more accurate predictions of organic matter flux in this climate-sensitive region.Subject terms: Microbial ecology, Virus-host interactions     

Primary and new production in the deep Canada Basin during summer 2002

The NOAA Ocean Exploration program provided the opportunity to measure the carbon and nitrogen productivity across the Canada Basin. This research examined the major environmental factors limiting the levels of primary production and possible future climate change on the ecosystems. The vertical distributions of the carbon and nitrogen uptakes of phytoplankton had similar patterns as their respective biomass concentrations which were low at the surface and highest in the chlorophyll-maximum layer. The annual carbon and new production rates of phytoplankton in the Canada Basin were about 5 and 1 g C m^–2, respectively. Nutrients were determined to be a main limiting factor at the surface, whereas light may be a major factor limiting phytoplankton productivity in the chlorophyll-maximum layer for open waters. The bottom surface of the ice has a low specific uptake and productivity of phytoplankton, indicating that photosynthetic activity might be controlled by both light and nutrients.     

ANTARCTIC AQUATIC ECOSYSTEMS AS HABITATS FOR PHYTOPLANKTON

1. The Southern Ocean is a large-scale, relatively homogeneous upwelling ecosystem whose phytoplankton apparently grows suboptimally over much of its area. By contrast there is a wide variety of freshwater habitats in the Antarctic and in some of these phytoplankton growth efficiency is very high. The two habitats share similar temperature and irradiance regimes, but differ markedly in availability of inorganic nutrients, in grazing pressure and in the time- and space-scales on which various physical processes act. 2. Concentrations of inorganic nutrients in the marine ecosystem have been represented as being in excess of phytoplankton requirements, but the ionic composition of some nutrient pools may not conform to phytoplankton preferences. 3. Nutrient-limitation determines phytoplankton production in Antarctic lakes and gives rise to gross differences between lakes. 4. Irradiance in the water column varies greatly over the year in both marine and freshwater ecosystems. Most algae are shade-adapted, with the ability to utilize low irradiance but with sub-optimal response to high irradiance. However, local phytoplankton maxima may attain very high carbon fixation and growth rates. 5. Consistently low temperatures characterize both systems. Their effects on photo-synthetic carbon uptake mirror shade-adaptation. Division rates of marine phytoplankton may however be very much higher than predicted for ambient temperatures. 6. Vertical mixing is important in both ecosystems and influences the environment experienced by phytoplankton cells. This appears to have little effect on the average performance of phytoplankton in the strongly mixed surface water column of the Southern Ocean, where the mixed depth may exceed 100 m. This can be related partly to the shade-adapted photosynthetic response. Euphotic depths range from 20 to 100 m. 7. Strong vertical mixing under ice-free conditions in lakes may maximize photosynthetic efficiency, whilst distinct vertical stratification in permanently ice-covered lakes gives rise to segregation of nutrient uptake and regeneration. 8. Physical removal of phytoplankton biomass by grazing is locally important in the Southern Ocean, in contrast to the estimated mean mesoscale impact of grazing. Vertical sedimentation losses appear important in the context of mixing depth and generation time, and may be modified by vertical circulation of water. 9. Loss of phytoplankton biomass from lakes during the ice-free period is dominated by physical removal via the lake outflow. Grazing is generally unimportant, except where larvae of otherwise nektobenthic zooplankton hatch in synchrony with a phytoplankton maximum. Sedimentation is important under ice-cover.     

Linking Land and Sea: Different Pathways for Marine Subsidies

Nutrients and energy derived from marine autotrophs subsidize shore ecosystems, increasing productivity and affecting food web dynamics and structure. In this study we examined how the inland reach of such inflow effects depends on vectors carrying the marine inflow inland and on landscape structure. We used stable isotopes of carbon and nitrogen to examine the roles of arthropod vectors in carrying marine-derived nutrients inland in two very different shore ecosystems: shore meadows in Sweden with marine inflows of algae and emerging chironomid midges; and sandy beaches and shore dunes in south-western Australia with marine inflows of algae and seagrass. In a colonization experiment, we found that deposited wrack on the beach is quickly colonized by both grazers and predators. However, in both systems we found a larger inland reach of the marine subsidy than could be accounted for by deposited macrophytes on shores alone, and that dipterans and spiders potentially functioned as vectors for the inflow. Our results indicate that marine inflows are important for near-shore terrestrial ecosystems well above the water’s edge, and that this effect is largely due to arthropod vectors (mainly dipterans and spiders) in both low-productivity sandy beach ecosystems at the Indian Ocean coast of Australia, and more productive shore meadows on the Baltic Sea coast of Sweden. Our findings also suggest that the type of vector transporting marine material inland may be as important as the productivity contrast between ecosystems for explaining the degree of marine influence on the terrestrial system.     

Abundance and function of bacteria in the Southern Ocean.

The very low water temperatures existing in polar oceans that experience seasonal advance and retreat of pack ice do not inhibit the presence of large bacterial populations. Bacteria may contribute significantly to the energy transfers within the Southern Ocean. In the last decades, notable progress has been made in the knowledge of the role of marine bacteria in the Southern Ocean. A short overview of the abundance and function ofAntarctic marine bacteria is given, with respect to metabolic activity. The importance of spatial and temporal variability is described. The ecological function of Antarctic marine bacterioplankton is discussed. Depending on food web structure, bacteria may be either a link in food webs supporting metazoan production, or a sink where bacterial production is metabolised by microorganisms. In the more oligotrophic areas and during certain periods of the year bacterial biomass dominates phytoplankton. The microbial food web is therefore the dominant pathway for carbon and energy flow in Antarctic seawater.     

A phytoplankton absorption-based primary productivity model for remote sensing in the Southern Ocean

Recent global environmental changes such as an increase in sea surface temperature (SST) are likely to impact primary productivity of phytoplankton in the Southern Ocean. However, models to estimate net primary production using satellite data use SST and uncertain estimation of chlorophyll a (chl-a) concentration. A primary productivity model for satellite ocean color data from the Southern Ocean, which is based on the light absorption coefficient of phytoplankton to reduce uncertainties of sea surface chl-a estimations and bias in optimal values of chl-a normalized productivity derived from SST, has been developed. The new model was able to estimate net primary productivity in the water column (PP _eu) without dependency on temperature when in the range of −2 to 25°C, and it explained 51% of the observed variability in PP _eu with a root mean square error (RMSE) of 0.15. Application of the model revealed that the SST dependent model has overestimated PP _eu in warmer waters around the Subtropical Front, and underestimated PP _eu in colder waters poleward of the Sub-Antarctic Front. This absorption-based primary productivity model contributes to a study of the relationship among spatio-temporal variations in the physical environment, and biogeochemical cycles in the Southern Ocean.     

Comparison of sterol and fatty acid profiles of chytrids and their hosts reveals trophic upgrading of nutritionally inadequate phytoplankton by fungal parasites

Chytrids are ubiquitous fungal parasites in aquatic ecosystems, infecting representatives of all major phytoplankton groups. They repack carbon from inedible phytoplankton hosts into easily ingested chytrid propagules (zoospores), rendering this carbon accessible to zooplankton. Grazing on zoospores may circumvent bottlenecks in carbon transfer imposed by the dominance of inedible or poorly nutritious phytoplankton (mycoloop). We explored qualitative aspects of the mycoloop by analysing lipid profiles (fatty acids, sterols) of two chytrids infecting two major bloom-forming phytoplankton taxa of contrasting nutritional value: the diatom Asterionella formosa and the filamentous cyanobacterium Planktothrix agardhii. The polyunsaturated fatty acid composition of chytrids largely reflected that of their hosts, highlighting their role as conveyors of otherwise inaccessible essential lipids to higher trophic levels. We also showed that chytrids are capable of synthesizing sterols, thus providing a source of these essential nutrients for grazers even when sterols are absent in their phytoplankton hosts. Our findings reveal novel qualitative facets of the mycoloop, showing that parasitic chytrids, in addition to making carbon and essential lipids available from inedible sources, also upgrade their host's biochemical composition by producing sterols de novo, thereby enhancing carbon and energy fluxes in aquatic food webs.     

海洋浮游植物与生物碳汇

系统描述了浮游植物与海洋碳汇相关的几个过程:初级生产、浮游植物沉降、浮游动物粪球打包沉降、经典食物链碳汇、溶解有机碳生产和转化、透明胞外聚合颗粒物(TEP)凝聚网,和CO₂分压升高(海水酸化)影响下浮游植物功能群转变及中国海可能的生物碳汇前景展望。提出海洋初级生产过程和TEP凝聚网过程是中国海生物碳汇的关键过程,而中国海的黄海中部及长江口区域是生物碳汇研究的重点区域,建议将硅藻及其碳汇过程作为今后研究的重点。     

Community Structure of Tintinnid Ciliates of the Microzooplankton in the South West Pacific Ocean: Comparison of a High Primary Productivity with a Typical Oligotrophic Site

Transient ‘hot spots’ of phytoplankton productivity occur in the generally oligotrophic Southern Pacific Ocean and we hypothesized that the population structure of tintinnid ciliates, planktonic grazers, would differ from that of a typical oligotrophic sites. Samples were collected over a 1‐wk period at each of two sites between Fiji and Tahiti: one of elevated chlorophyll a concentrations and primary productivity with an abundance of N‐fixing cyanobacteria Trichodesmium, and a distant oligotrophic site. Tintinnid abundance differed between the sites by a factor of 2. A single species (Favella sp.), absent from the oligotrophic site, highly dominated the ‘hot spot’ site. However, total species richness was identical (71 spp.) as well as short‐term temporal variability (2–4 d). At both sites, species abundance distributions most closely fit a log‐series or log‐normal distribution and the abundance distributions of ecological types, forms of distinct lorica oral diameter, were the typical geometric. Morphological diversity was only slightly lower at the high productivity site. We found that communities of these plankton grazers in ‘hot spots’ of phytoplankton productivity in oligotrophic systems, although harboring different species, differ little from surrounding oligotrophic areas in community structure.     

海洋生态系统固碳能力估算方法研究进展

气候变化受到全球关注,大气中CO2含量与气候变化息息相关。海洋是地球上最大的活跃碳库,在气候变化中扮演着举足轻重的作用。定量估算海洋中碳元素的吸收、转移、埋藏速率在全球碳循环及全球气候变化研究中有重要意义。目前,海洋固碳能力估算研究包括:利用海-气界面CO2分压差法估算海洋海-气界面CO2交换通量,根据海水中叶绿素含量建立的生态学数理模型法估算真光层浮游生物的初级生产力,234Th—238U不平衡法估算POC输出通量,210Pb定年法估算有机碳沉积通量。但迄今为止的研究工作尚有一定局限性,碳在大气—海水—沉积物3种介质间交换通量间相互影响的研究较少,海洋中碳垂直传输过程的主要影响因素和关键控制因子尚不明确,在海洋生态系统固碳能力估算方法方面国内外还没有统一的规范和标准。为进一步完善海洋生态系统固碳能力的估算方法,今后的工作应注重海洋固碳整套观测技术、分析和估算方法研究,并建立海洋碳汇估算指标体系、指标标准体系、以及评价标准体系,为我国的碳"减排"、"增汇"国家需求提供技术支持。     

铁施肥促进海洋浮游植物和生物碳泵的不确定性

铁作为浮游植物所必需的微量元素,限制了全球超过三分之一海域的初级生产力,尤其是在高营养盐、低叶绿素海域(high nutrient low chlorophyll,HNLC)。长期以来海洋铁施肥被认为是一项可以降低大气二氧化碳含量的地球工程策略。然而通过13次海洋人工铁施肥(artificial ocean iron fertilization,aOIF)实验发现,铁的额外添加对海洋深层碳输出量的促进作用要显著低于预期。本文简要地总结了碳在海洋和大气中的循环过程,回顾了人工铁施肥实验对生物碳泵和碳通量等的影响,分析了从海洋铁施肥到海洋碳汇关键生物地球化学过程的影响因素。综上分析发现,科学界对生物碳泵过程及其调控机制的认识仍十分浅薄,考虑到海洋铁施肥还会对海洋生态系统带来一定的负面作用,铁施肥能否作为降低大气中CO₂的有效手段,以达到碳中和并缓解温室效应仍需进一步研究。