Krill Population Research Articles

A unique warm–water oasis in the Siberian Arctic’s Chaun Bay sustained by hydrothermal groundwater discharge

Chaun Bay, located on the fringe of the East Siberian Sea, has been described since the mid-20th century to support a unique marine ecosystem that is atypical for the local Siberian Arctic. Here we use ship-board physical, biogeochemical and geological measurements taken in October 2020, along with hydrographic observations taken from land-fast ice in April 2023, to demonstrate that these warm-water biological communities are supported by hydrothermal submarine groundwater discharge that delivers heat, salinity, nutrients, and trace elements to the bay. We identify a cyclonic eddy that mixes the warm nutrient-rich groundwater with oxygen-rich surface water, resulting in a water mass within Chaun Bay that has similar physical and chemical properties to the highly productive waters of the North Pacific and Southern Chukchi Sea. The bay showed elevated concentrations of chlorophyll-a and zooplankton, and the abundance and species diversity of epibenthos significantly exceeded values observed elsewhere in the East Siberian Sea. The benthic communities contained a number of boreal species that are not typically found in the Arctic Ocean. We also observed Thysanoessa krill populations, a pelagic species generally considered an expatriate in Arctic waters.

Factors impacting the timing of reproductive development in female Antarctic krill at the northwestern Antarctic Peninsula

The northwestern Antarctic Peninsula is an important spawning, recruitment, and overwintering ground for Antarctic krill. The region is warming rapidly, and the current impacts of climate and environmental variability on the reproductive cycle of krill remain unclear. Here, we examine the reproductive stage of female krill in the austral winter from 2012 to 2016 in relation to climate and environmental data to assess what factors influence the timing of reproductive development. We observed significant interannual variability in the degree of maturation in female krill, ranging from 48% of female krill measured at a station in 2016 to a maximum of 94% of female krill measured at a station in 2014. On average, across all five years, three-quarters of the female krill sampled were in the stage known as previtellogenesis, the point at which the onset of sexual maturity begins. The preceding spring, summer, and autumn Southern Annular Mode and the Multivariate El Niño Index explained most of the variance in the data and indicated a strong, preconditioning storm-related effect on environmental conditions leading up to winter, affecting krill maturation status at the end of the winter season. Results from our study can be used to improve krill population models that are necessary for the management of the krill fishery and for conservation at the northwestern Antarctic Peninsula.

Interactions between krill and its predators in the western Ross Sea

Krill is a fundamental resource in the pelagic food web of the Ross Sea, constituting an important link between primary production and top predators. A series of Italian research voyages to the Ross Sea from 1994 to 2016 have contributed to our understanding of the dynamics of krill populations inhabiting the Ross Sea. Only the surveys in 1994 and 2004 reported information on krill’s predators through visual census data, and 2004 data were not object of publication until now. Analyzing Euphausia superba and Euphausia crystallorophias abundance spatial distribution in the study area in relation to the distribution of its key natural predators have shown a significant relationship between the spatial distribution of minke whales’ abundance and the density of E. superba biomass, indicating a classical predator-prey interaction. Moreover, krill biomass density data in the water column were analyzed together with the main environmental data from CTD samplings. The analysis of krill density data in relation to environmental factors throughout the water column revealed a significant relation between E. superba abundance and salinity, a result that may be linked to the presence of ice melting effects improving environment productivity conditions.

Blue Whale and Krill Populations Modeling

Blue Whale and Krill Populations Modeling

The impact of salps (Salpa thompsoni) on the Antarctic krill population (Euphausia superba): an individual-based modelling study

BackgroundKrill (Euphausia superba) and salps (Salpa thompsoni) are key macrozooplankton grazers in the Southern Ocean ecosystem. However, due to differing habitat requirements, both species previously exhibited little spatial overlap. With ongoing climate change-induced seawater temperature increase and regional sea ice loss, salps can now extend their spatial distribution into historically krill-dominated areas and increase rapidly due to asexual reproduction when environmental conditions are favorable. Understanding the potential effects on krill is crucial, since krill is a species of exceptional trophic significance in the Southern Ocean food web. Negative impacts on krill could trigger cascading effects on its predators and prey. To address this question, we combined two individual-based models on salps and krill, which describe the whole life cycle of salp individuals and the dynamic energy budget of individual krill. The resulting new model PEKRIS (PErformance of KRIll vs. Salps) simulates a krill population for 100 years under varying chlorophyll-a concentrations in the presence or absence of salps.ResultsAll of the investigated krill population properties (abundance, mean length, and yearly egg production) were significantly impacted by the presence of salps. On the other hand, salp density was not impacted if krill were present. The medians of krill population properties deviated during variable maximum chlorophyll-a density per year when salps were introduced by − 99.9% (− 234 individuals per 1000 m3) for krill density, − 100% (− 22,062 eggs per 1000 m3) for krill eggs and − 0.9% (− 0.3 mm) for mean length of krill.ConclusionsIf both species compete for the same food resource in a closed space, salps seem to inhibit krill populations. Further simulation studies should investigate whether this effect prevails if different phytoplankton sizes and consumption preferences of krill are implemented. Furthermore, direct predation of the two species or consumption of krill fecal pellets by salps could change the impact size of the food competition.

Environmental and behavioural drivers of Antarctic krill distribution at the South Orkney Islands: A regional perspective

Antarctic krill (Euphausia superba) is a key species in the marine ecosystem of the Southern Ocean, but is also the target of a commercial fishery, with an important fishing ground in the South Orkney Islands region. The potential for competition for krill between predators and the fishery requires risk management strategies for the fishery, underpinned by an understanding of the key physical and behavioural drivers of krill movement and retention in target areas. Here, we present the results of a regional modelling study, combining a high-resolution ocean-sea ice model and an individual-based model parameterised for krill, to elucidate the roles of oceanographic variability and krill behaviour on patterns of transport and retention on and around the South Orkney Plateau. Simulations suggest that oceanic transport from sources around the Antarctic Peninsula is restricted by the northward flowing Antarctic Slope Current. Around the South Orkney Plateau, anticyclonic flows associated with the Weddell Front and the shelf edge transport krill rapidly towards the main fishing grounds to the northwest of the plateau. Transport onto the shelf and subsequent retention are influenced by the strength and direction of regional winds; weaker on-shelf transport and shorter retention times are associated with stronger westerly and northerly winds. The incorporation of sea-ice associated behaviour, whereby krill are moved with sea ice when sea ice is present, significantly modifies the patterns from purely oceanic transport; it reduces the influence of strong regional oceanic flows and increases transport of krill to the South Orkneys region from the Antarctic Peninsula. The inclusion of diel vertical migration also modifies predicted patterns from oceanic transport, but to a lesser extent, and moderates the impact of including sea-ice associated behaviour. We highlight the importance of understanding the behaviour of krill, including age-dependent behavioural changes in response to sea ice conditions, for modelling and management of Antarctic krill populations.

Krill body size drives particulate organic carbon export in West Antarctica.

The export of carbon from the ocean surface and storage in the ocean interior is important in the modulation of global climate1-4. The West Antarctic Peninsula experiences some of the largest summer particulate organic carbon (POC) export rates, and one of the fastest warming rates, in the world5,6. To understand how warming may alter carbon storage, it is necessary to first determine the patterns and ecological drivers of POC export7,8. Here we show that Antarctic krill (Euphausia superba) body size and life-history cycle, as opposed to their overall biomass or regional environmental factors, exert the dominant control on the POC flux. We measured POC fluxes over 21 years, the longest record in the Southern Ocean, and found a significant 5-year periodicity in the annual POC flux, which oscillated in synchrony with krill body size, peaking when the krill population was composed predominately of large individuals. Krill body size alters the POC flux through the production and export of size-varying faecal pellets9, which dominate the total flux. Decreases in winter sea ice10, an essential habitat for krill, are causing shifts in the krill population11, which may alter these export patterns of faecal pellets, leading to changes in ocean carbon storage.

ИСПОЛЬЗОВАНИЕ РАЗРАБАТЫВАЕМОЙ АВТОНОМНОЙ РОБОТОТЕХНИЧЕСКОЙ СИСТЕМЫ «МОБИЛЬНЫЙ БИОЛОГ» ДЛЯ ИССЛЕДОВАНИЯ ЭКОСИСТЕМЫ АНТАРКТИКИ

The paper addresses the issues of using the developed autonomous robotic system to study the influence of water dynamics parameters on the density of Antarctic krill accumulations in traditional areas. With the help of this system, potentially vulnerable natural and ecological habitats of Antarctic krill can be identified, based on the data from which solutions for their conservation and stabilization can be proposed. An autonomous robotic system allows for such continuous monitoring to observe the basic trophic levels of ecosystems, the effects of changes in sea ice conditions, and other Antarctic environmental factors affecting the marine ecosystem. The application of the proposed method allows simultaneous measurements of environmental parameters in order to assess the relationship between the physical parameters of sea currents and biological processes. By integrating the system data with ship and satellite data in postprocessing, the response of Antarctic krill populations to multifactorial stresses can be assessed. The work was carried out according to the state assignment No. 0128-2021-0002 (“Mechanisms for the formation of the circulation structures of the World Ocean: key processes in the boundary layers and their role in ocean dynamics based on expeditionary studies, numerical and laboratory modeling”).

Impact of the climate regime shift around 2000 on recruitment of Antarctic krill at the Antarctic Peninsula and South Georgia

We examined how the climate regime shift around 2000 affected Antarctic krill recruitment variability at the North Antarctic Peninsula (NAP) and South Georgia (SG) during the period of 1990s through to 2000s. We used sea surface temperature (SST) as a proxy of the monthly sea ice extent and related it to the recruitment index (proportion of 1-year-old krill) of each succeeding year for NAP and SG by examining the correlation of the time series before and after 2000. For NAP, recruitment index was negatively correlated with winter SST at NAP in the 1990s but with autumn SST in the 2000s, suggesting that good recruitment was supported by extensive winter sea-ice in the 1990s but by extensive autumn sea-ice in the 2000s. This was attributed to the regime shift featured by winter warming and autumn cooling after 2000. For SG, recruitment was negatively correlated with winter SST at NAP in the 1990s but positively correlated with autumn SST in the southern Scotia Sea (SSS) in the 2000s. According to particle tracking experiment from NAP to SG in relation to the sea-ice extent and position of SACCF (Southern Antarctic Circumpolar Current Front), less sea-ice extent in 2000s meant less larvae distributing as north as SACCF, resulting in much fewer larval being transported to SG. Hence, we hypothesized that the regime shift weakened the connection between NAP and SG, but instead SSS became the main driver of recruitment at SG. We presume the krill population demonstrated adaptability to the regime shift by offsetting the unfavorable winter condition with the favorable autumn condition at NAP and for SG, replacing the source of recruits with those closer to it.

The enormous repetitive Antarctic krill genome reveals environmental adaptations and population insights

Antarctic krill (Euphausia superba) is Earth's most abundant wild animal, and its enormous biomass is vital to the Southern Ocean ecosystem. Here, we report a 48.01-Gb chromosome-level Antarctic krill genome, whose large genome size appears to have resulted from inter-genic transposable element expansions. Our assembly reveals the molecular architecture of the Antarctic krill circadian clock and uncovers expanded gene families associated with molting and energy metabolism, providing insights into adaptations to the cold and highly seasonal Antarctic environment. Population-level genome re-sequencing from four geographical sites around the Antarctic continent reveals no clear population structure but highlights natural selection associated with environmental variables. An apparent drastic reduction in krill population size 10 mya and a subsequent rebound 100 thousand years ago coincides with climate change events. Our findings uncover the genomic basis of Antarctic krill adaptations to the Southern Ocean and provide valuable resources for future Antarctic research.

Alkenone Uk’37 index differs between thermally separated populations of fin whales and krill

Although habitat temperature is an important determinant of species distributions, its measurement is difficult in mobile marine organisms. Chemical tracers such as alkenones constitute an alternative tool for gauging marine habitat temperature, something particularly relevant in the current scenario of global warming. The unsaturation index of alkenones, the Uk’37 index, can be used to estimate sea surface temperature (SST) in living organisms. Here, we analyse alkenone concentrations in a predator species, the fin whale, and its prey, the northern krill, both sampled in 2 areas with different SSTs: SW Iceland and NW Spain. In NW Spain (but not in SW Iceland), alkenone concentrations were higher in krill than in fin whale blubber, suggesting that they may biodilute along the trophic transfer. Consistently with local SST, the Uk’37 index was lower in the Icelandic samples of both fin whales and krill than in those from NW Spain, confirming the ability of this index to distinguish populations that are thermally separated. Whales are migratory animals; thus, the alkenones present in their blubber are a mix of those ingested locally and in recently visited regions. Consistently, the Uk’37 index showed a higher correlation with the local SST in krill than in fin whales. Alkenone turnover rates should be considered when using this proxy to assess the thermal range of the feeding habitat of a species. We conclude that the Uk’37 index is a potentially efficient tool to study the behaviour of whales, thus providing an alternative perspective to other chemical tracers.

Acoustic sampling of Antarctic krill with simulated underwater buoyancy gliders: Does the sawtooth dive pattern work?

Autonomous underwater gliders may be viable adjuncts to or in some cases replacements for ship-based oceanographic sampling. Gliders and ships acoustically sample the water column differently, with ships sampling all depths simultaneously in a single vertical pulse and gliders sampling shorter vertical segments of the water column in an up and down, sawtooth pattern. We simulated gliders following this flight pattern to sample the densities at depth of Antarctic krill (Euphausia superba), a patchily-distributed crustacean that is targeted by an international fishery. Krill densities from ship-based surveys conducted between 2001 to 2011 were treated as the “true” population densities sampled by the simulated gliders. Depth-integrated densities estimated from the glider sampling were compared to the population densities for each year. Coverage probabilities (the proportion of population means within a standard deviation of the glider sample means) for gliders diving to 150 m were near 100% in most years, better than the nominal 68%. Gliders diving to a maximum depth of 150 m estimated the annual population means better than gliders diving deeper because shallow dives provided more samples for a given length of trackline. Modeling the zero and non-zero data as separate distributions (the delta approach), an alternative to the lognormal CV approach used in this study, resulted in less accurate estimates of krill population densities. These results suggest that the sawtooth flight pattern of gliders can produce density estimates of krill comparable to the annual time series of density estimates from ship-based surveys. Gliders may also be useful to survey other patchily-distributed pelagic organisms.

The energetic cost of early reproductive development in juvenile Antarctic krill at the Western Antarctic Peninsula

The overwinter survival mechanisms of Antarctic krill, Euphausia superba, are poorly characterized, especially for juveniles. It has been suggested that juveniles adopt a mix of strategies characteristic of both larvae and adults. Like larvae, they may feed opportunistically throughout winter when food is available, and like adults they may be able to suppress their metabolism when food is scarce. In this study we look at the overwinter strategies of juvenile krill and how their reproductive development changes when energy input exceeds what is necessary for survival. We take a closer look at how the sexual maturation of juvenile krill progresses in response to different environmental conditions throughout the fall and winter. We exposed juvenile Antarctic krill to four different “food environment scenarios”, supplementing them with various diets from May to September 2019 that were representative of environmental conditions that they may encounter in different regions of the Western Antarctic Peninsula during autumn and winter. Each month, we measured the physiology and condition of the krill, and assessed the reproductive development of females. We found that when female juvenile krill have greater energy reserves than what is needed to survive the winter, they will begin to sexually mature. Further, when there are sufficient levels of the fatty acids eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA) and 16:4 (n-1), krill are likely to be in a more reproductive advanced stage. However, when lipids, EPA, DHA and 16:4 (n-1) are depleted throughout the winter, juvenile female krill lose their ability to develop reproductively. We also found that sexual development is an energy intensive process that requires high respiration rates in juvenile krill. Furthermore, when juvenile females expend energy maturing, their physiological condition declines. This trade-off between early reproductive development and condition in juvenile female krill has important implications for individual health and population fecundity. Gaining a better understanding of the mechanisms behind juvenile krill winter survival strategies and their consequences will allow us to predict how future change at the western Antarctic Peninsula may affect krill population dynamics, especially in light of a warming climate.

Distribution and Demography of Antarctic Krill and Salps in the Atlantic Sector of the Southern Ocean during Austral Summer 2021–2022

The study aimed to investigate krill (Euphausia superba) and salp (Salpa thompsoni) populations in the Atlantic sector of the Southern Ocean in January and February 2022. Samples were obtained to measure the abundance, biomass and distribution patterns of krill and salp. Sex differences and feeding habits of the Antarctic krill were determined. The dependence of the physiological state of the studied aquatic organisms on changes in environmental parameters was analyzed. Current data on the association of the dynamics of hydrometeorological parameters and processes with the distribution of chlorophyll a, krill, and salp were obtained. It was established that, at numerous stations, the biomass of salps prevailed over krill. The result indicates the replacement of the Antarctic krill populations by gelatinous zooplankton. The obtained results allow assessment of the biological resource potential in the studied region based on the analysis of the samples collected.

Composition and Distribution of Plankton Communities in the Atlantic Sector of the Southern Ocean

In recent decades, the waters off the Antarctic Peninsula and surrounding region have undergone a significant transformation due to global climate change affecting the structure and distribution of pelagic fauna. Here, we present the results of our study on the taxonomic composition and quantitative distribution of plankton communities in Bransfield Strait, Antarctic Sound, the Powell Basin of the Weddell Sea, and the waters off the Antarctic Peninsula and South Orkney Islands during the austral summer of 2022. A slight warming of the Transitional Zonal Water with Weddell Sea influence (TWW) and an increase in its distribution area was detected. Among the pelagic communities, three groups were found to be the most abundant: copepods Calanoides acutus, Metridia gerlachei, and Oithona spp., salpa Salpa thompsoni, and Antarctic krill Euphausia superba. Euphausiids were found in cases of low abundance, species diversity, and biomass. In the studied region, an increase in the amount of the salpa S. thompsoni and the euphausiid Thysanoessa macrura and the expansion of their distribution area were observed. Significant structural shifts in phytoplankton communities manifested themselves in changes in the structure of the Antarctic krill forage base. The composition and distribution of pelagic fauna is affected by a combination of environmental abiotic factors, of which water temperature is the main one. The obtained results have allowed us to assume that a further increase in ocean temperature may lead to a reduction in the number and size of the Antarctic krill population and its successive replacement by salps and other euphausiids that are more resistant to temperature fluctuations and water desalination.

Projecting environmental and krill fishery impacts on the Antarctic Peninsula food web in 2100

The Antarctic Peninsula ecosystem is extremely sensitive to climatic variability and other anthropogenic perturbances ascribed to biomass extraction by fisheries. An Ecopath with Ecosim model calibrated for the 1996–2012 period was projected into the future (2100) under three different climate projections for environmental variables (sea ice extent, open water area and chlorophyll-a concentration) and three Antarctic krill fishery scenarios (no-take, constant and decadal increase until doubling of the current catches). The relative impact of different drivers controlling Antarctic food web dynamics was evaluated with a sensitivity analysis and the temporal variability of several functional group and ecosystem indicators. Under these scenarios, environmental variability resulted in a greater impact on the Antarctic food web in 2100 projections compared with the krill fishery. Chlorophyll-a biomass strongly influenced the temporal variability of functional groups, suggesting predominant bottom-up control on the food web. An alternative food web structure was observed in 2100, with a marked decline in krill population biomass (from<50% to near extinction depending on the environmental projection) and an increase in salps and other zooplankton groups. A reduction in the biomass of sea ice and krill-dependent predators, such as Adélie and chinstrap penguins and crabeater seals, was also observed. The absence of functions modelling the spatial and seasonal variability of the krill fishery might cause an underestimation of its ecosystem impacts. This work provides useful insights into the dynamic responses of the Antarctic food web under likely environmental projections and highlights critical points that need to be addressed to improve the understanding and parametrization of the Antarctic food web to anticipate future variability.

UAV path planning based on an elite-guided orthogonal diagonalised krill herd algorithm

At present, obstacle avoidance and the shortest path to the destination are the main problems that need to be considered when the UAV (unmanned aerial vehicle) performs its mission. In this paper, an Elite-Guided Orthogonal Diagonalised Krill Herd (EODKH) algorithm is developed to solve the path planning problem of UAV in three-dimensional space with complex terrain. EODKH algorithm divides the krill population into two parts: one part is composed of elite krill, and the evolution of krill population is guided by the experience of elite krill with orthogonal diagonalisation, and the elite krill with higher rank can obtain greater 'respect' in the evolution procedure; the other part evolves according to the original krill herd method, so as to improve the convergence diversity of the whole krill herd. Experimental results show that EODKH is better than other krill herd algorithms in UAV path planning.

Lingering Chukchi Sea sea ice and Chukchi Sea mean winds influence population age structure of euphausiids (krill) found in the bowhead whale feeding hotspot near Pt. Barrow, Alaska.

Interannual variability in euphausiid (krill) abundance and population structure and associations of those measures with environmental drivers were investigated in an 11-year study conducted in late August–early September 2005–2015 in offshelf waters (bottom depth > 40 m) in Barrow Canyon and the Beaufort Sea just downstream of Distributed Biological Observatory site 5 (DBO5) near Pt. Barrow, Alaska. Statistically-significant positive correlations were observed among krill population structure (proportion of juveniles and adults), the volume of Late Season Melt Water (LMW), and late-spring Chukchi Sea sea ice extent. High proportions of juvenile and adult krill were seen in years with larger volumes of LMW and greater spring sea ice extents (2006, 2009, 2012–2014) while the converse, high proportions of furcilia, were seen in years with smaller volumes of LMW and lower spring sea ice extent (2005, 2007, 2010, 2011, 2015). These different life stage, sea ice and water mass regimes represent integrated advective responses to mean fall and/or spring Chukchi Sea winds, driven by prevailing atmospheric pressure distributions in the two sets of years. In years with high proportions of juveniles and adults, late-spring and preceding-fall winds were weak and variable while in years with high proportions of furcilia, late-spring and preceding-fall winds were strong, easterly and consistent. The interaction of krill life history with yearly differences in the northward transports of krill and water masses along with sea ice retreat determines the population structure of late-summer krill populations in the DBO5 region near Pt. Barrow. Years with higher proportions of mature krill may provide larger prey to the Pt. Barrow area bowhead whale prey hotspot. The characteristics of prey near Pt. Barrow is dependent on krill abundance and size, large-scale environmental forcing, and interannual variability in recruitment success of krill in the Bering Sea.

Overwinter sea-ice characteristics important for Antarctic krill recruitment in the southwest Atlantic

Climate change alters the extent and structure of sea-ice environments, which affects how they function as a habitat for polar species. Identifying sea-ice characteristics that serve as indicators of habitat quality will be crucial to the monitoring and management of climate change impacts. In the Southern Ocean, Antarctic krill is a key prey species and fishery target. Krill larvae depend upon sea-ice habitats to survive the winter and recruit to the population in spring. Existing observations of sea-ice characteristics lack sufficient spatiotemporal coverage to quantify which ones contribute to favourable overwintering habitat, leading to uncertainties in how current and future changes in sea ice affect krill populations. Here, we derive regional-scale indices of annual krill recruitment spanning 35 years across the southwest Atlantic. To develop meaningful indicators of sea-ice habitat, we selected variables from a high-resolution sea-ice model that are hypothesized as relevant for larval habitat use. The resulting correlations between recruitment and sea-ice indicators vary by region and show remote connections to sea ice that correspond with established theories of larval transport. Through an improved representation of sea-ice habitat quality, as compared with using more traditional satellite-derived variables such as sea-ice extent and duration, we highlight plausible regions of overwintering habitat. Our findings improve current understanding of how krill are likely responding to changing sea ice and support emerging views that larval habitat use is complex. Furthermore, regional variation in larval dependence on sea ice may provide pockets of resilience to change for the broader krill population.

Salp fecal pellets release more bioavailable iron to Southern Ocean phytoplankton than krill fecal pellets

Over the last decades, it has been reported that the habitat of the Southern Ocean (SO) key species Antarctic krill (Euphausia superba) has contracted to high latitudes, putatively due to reduced winter sea ice coverage, while salps as Salpa thompsoni have extended their dispersal to the former krill habitats. To date, the potential implications of this population shift on the biogeochemical cycling of the limiting micronutrient iron (Fe) and its bioavailability to SO phytoplankton has never been tested. Based on uptake of fecal pellet (FP)-released Fe by SO phytoplankton, this study highlights how efficiently krill and salps recycle Fe. To test this, we collected FPs of natural populations of salps and krill, added them to the same SO phytoplankton community, and measured the community's Fe uptake rates. Our results reveal that both FP additions yielded similar dissolved iron concentrations in the seawater. Per FP carbon added to the seawater, 4.8± 1.5 times more Fe was taken up by the same phytoplankton community from salp FP than from krill FP, suggesting that salp FP increased the Fe bioavailability, possibly through the release of ligands. With respect to the ongoing shift from krill to salps, the potential for carbon fixation of the Fe-limited SO could be strengthened in the future, representing a negative feedback to climate change.