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.

Hydrodynamics of the fast-start caridoid escape response in Antarctic krill, Euphausia superba.

Krill are shrimp-like crustaceans with a high degree of mobility and variety of documented swimming behaviors. The caridoid escape response, a fast-start mechanism unique to crustaceans, occurs when the animal performs a series of rapid abdominal flexions and tail flipping that results in powerful backward strokes. The current results quantify the animal kinematics and three-dimensional flow field around a free-swimming Euphausia superba as it performs the caridoid escape maneuver. The specimen performs a single abdominal flexion-tail flip combination that leads to an acceleration over a 42 ms interval allowing it to reach a maximum speed of 57.0 cm/s (17.3 body lengths/s). The krill's tail flipping during the abdominal closure is a significant contributor to the thrust generation during the maneuver. The krill sheds a complex chain of vortex rings in its wake due to the viscous flow effects while the organism accelerates. The vortex ring structure reveals a strong suction flow in the wake, which suggests that the pressure distribution and form drag play a role in the force balance for this maneuver. Antarctic krill typically swim in a low to intermediate Reynolds number (Re) regime where viscous forces are significant, but as shown by this analysis, its high maneuverability allows it to quickly change its body angle and swimming speed.

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.

Antarctic marine life under pressure.

Next week, the Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR) convenes in Hobart, Tasmania, to examine the state of marine life in the Southern Ocean. As part of the Antarctic Treaty System, this convention entered into force in 1982, and its focus on the region's environmental integrity has never been more important, given the increasing effects of climate change and commercial fishing. An important focus over the past 40 years has been Antarctic krill, Euphausia superba (hereafter krill), a keystone species that helps to hold this marine ecosystem together. Climate and fishing stresses should prompt the CCAMLR to address whether management of krill fishing is at a level that protects the Southern Ocean from losing its overall balance of marine life and the oceanic processes that regulate global climate.

A thorough annotation of the krill transcriptome offers new insights for the study of physiological processes.

The krill species Euphausia superba plays a critical role in the food chain of the Antarctic ecosystem. Significant changes in climate conditions observed in the Antarctic Peninsula region in the last decades have already altered the distribution of krill and its reproductive dynamics. A deeper understanding of the adaptation capabilities of this species is urgently needed. The availability of a large body of RNA-seq assays allowed us to extend the current knowledge of the krill transcriptome. Our study covered the entire developmental process providing information of central relevance for ecological studies. Here we identified a series of genes involved in different steps of the krill moulting cycle, in the reproductive process and in sexual maturation in accordance with what was already described in previous works. Furthermore, the new transcriptome highlighted the presence of differentially expressed genes previously unknown, playing important roles in cuticle development as well as in energy storage during the krill life cycle. The discovery of new opsin sequences, specifically rhabdomeric opsins, one onychopsin, and one non-visual arthropsin, expands our knowledge of the krill opsin repertoire. We have collected all these results into the KrillDB2 database, a resource combining the latest annotation of the krill transcriptome with a series of analyses targeting genes relevant to krill physiology. KrillDB2 provides in a single resource a comprehensive catalog of krill genes; an atlas of their expression profiles over all RNA-seq datasets publicly available; a study of differential expression across multiple conditions. Finally, it provides initial indications about the expression of microRNA precursors, whose contribution to krill physiology has never been reported before.

Biological-physical processes regulate autumn prey availability of spiny icefish Chaenodraco wilsoni in the Bransfield Strait, Antarctic.

This study examines the adaptability of a Southern Ocean predator, which is dependent on Antarctic krill (Euphausia superba), to potential changes in food availability. Muscle fatty acids (FAs) of the spiny icefish Chaenodraco wilsoni collected from three areas in the Bransfield Strait (BS), northern Antarctic Peninsula during February-April 2016 give a good representation of their feeding variability. The compositions of 22:6n3 (DHA) and 20:5n3 (EPA) were both higher in the Transitional Zonal Water with Bellingshausen influence (TBW)-controlled C. wilsoni than in the Transitional Zonal Water with Weddell Sea influence (TWW)-controlled fish. This was positively correlated with photoadaptation and carbon sequestration in TBW-controlled phytoplankton. Results for the FAs 16:1n7, 16:0, DHA and EPA indicate the presence of dinoflagellates in all three areas, suggesting that during late summer and early fall, there is a seasonal phytoplankton succession, where small phytoplankton become dominant, in the BS. In addition, the compositions of some long-chain FAs (>20, such as 20:0, 20:1, 22:0 and 22:1n9) and ∑18 indicated that the food chain based on flagellates and copepods was more apparent in TWW-controlled C. wilsoni, especially the effect of El Niño-Southern Oscillation (ENSO) on the variation of prey communities in TWW-controlled areas. FA markers such as SFA/(PUFA+MUFA), ∑15 + ∑17 and ARA were more pronounced in TWW-controlled C. wilsoni, indicating a more strongly carnivorous and benthic food source. In the TBW-TWW confluence, the complex hydrological structure, including the presence of a large number of mesoscale eddies, allows rich nutrients and krill larvae to remain in it, providing a rich food source for the C. wilsoni. Overall, the FA data of this study show that the diet of C. wilsoni varies in different marine environments, aiding their survivability at the face of climate change.

Self-organization and information transfer in Antarctic krill swarms.

Antarctic krill swarms are one of the largest known animal aggregations, and yet, despite being the keystone species of the Southern Ocean, little is known about how swarms are formed and maintained. Understanding the local interactions between individuals that provide the basis for these swarms is fundamental to knowing how swarms arise in nature, and what potential factors might lead to their breakdown. Here, we analysed the trajectories of captive, wild-caught krill in 3D to determine individual-level interaction rules and quantify patterns of information flow. Our results demonstrate that krill align with near neighbours and that they regulate both their direction and speed relative to the positions of groupmates. These results suggest that social factors are vital to the formation and maintenance of swarms. Furthermore, krill operate a novel form of collective organization, with measures of information flow and individual movement adjustments expressed most strongly in the vertical dimension, a finding not seen in other swarming species. This research represents a vital step in understanding the fundamentally important swarming behaviour of krill.

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.

Photophysiological cycles in Arctic krill are entrained by weak midday twilight during the Polar Night.

Light plays a fundamental role in the ecology of organisms in nearly all habitats on Earth and is central for processes such as vision and the entrainment of the circadian clock. The poles represent extreme light regimes with an annual light cycle including periods of Midnight Sun and Polar Night. The Arctic Ocean extends to the North Pole, and marine light extremes reach their maximum extent in this habitat. During the Polar Night, traditional definitions of day and night and seasonal photoperiod become irrelevant since there are only "twilight" periods defined by the sun's elevation below the horizon at midday; we term this "midday twilight." Here, we characterize light across a latitudinal gradient (76.5° N to 81° N) during Polar Night in January. Our light measurements demonstrate that the classical solar diel light cycle dominant at lower latitudes is modulated during Arctic Polar Night by lunar and auroral components. We therefore question whether this particular ambient light environment is relevant to behavioral and visual processes. We reveal from acoustic field observations that the zooplankton community is undergoing diel vertical migration (DVM) behavior. Furthermore, using electroretinogram (ERG) recording under constant darkness, we show that the main migratory species, Arctic krill (Thysanoessa inermis) show endogenous increases in visual sensitivity during the subjective night. This change in sensitivity is comparable to that under exogenous dim light acclimations, although differences in speed of vision suggest separate mechanisms. We conclude that the extremely weak midday twilight experienced by krill at high latitudes during the darkest parts of the year has physiological and ecological relevance.

Selective feeding in Southern Ocean key grazers-diet composition of krill and salps.

Over the past decades, two key grazers in the Southern Ocean (SO), krill and salps, have experienced drastic changes in their distribution and abundance, leading to increasing overlap of their habitats. Both species occupy different ecological niches and long-term shifts in their distributions are expected to have cascading effects on the SO ecosystem. However, studies directly comparing krill and salps are lacking. Here, we provide a direct comparison of the diet and fecal pellet composition of krill and salps using 18S metabarcoding and fatty acid markers. Neither species' diet reflected the composition of the plankton community, suggesting that in contrast to the accepted paradigm, not only krill but also salps are selective feeders. Moreover, we found that krill and salps had broadly similar diets, potentially enhancing the competition between both species. This could be augmented by salps' ability to rapidly reproduce in favorable conditions, posing further risks to krill populations.

Individual and population dietary specialization decline in fin whales during a period of ecosystem shift.

This study sought to estimate the effect of an anthropogenic and climate-driven change in prey availability on the degree of individual and population specialization of a large marine predator, the fin whale (Balaenoptera physalus). We examined skin biopsies from 99 fin whales sampled in the St. Lawrence Estuary (Canada) over a nine year period (1998-2006) during which environmental change was documented. We analyzed stable isotope ratios in skin and fatty acid signatures in blubber samples of whales, as well as in seven potential prey species, and diet was quantitatively assessed using Bayesian isotopic models. An abrupt change in fin whale dietary niche coincided with a decrease in biomass of their predominant prey, Arctic krill (Thysanoessa spp.). This dietary niche widening toward generalist diets occurred in nearly 60% of sampled individuals. The fin whale population, typically composed of specialists of either krill or lipid-rich pelagic fishes, shifted toward one composed either of krill specialists or true generalists feeding on various zooplankton and fish prey. This change likely reduced intraspecific competition. In the context of the current "Atlantification" of northern water masses, our findings emphasize the importance of considering individual-specific foraging tactics and not only population or group average responses when assessing population resilience or when implementing conservation measures.

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.

Facing Southern Ocean warming: Temperature effects on whole animal performance of Antarctic krill (Euphausia superba).

The ongoing environmental changes in the Southern Ocean may cause a dramatic decrease in habitat quality. Due to its central position in the food web, Antarctic krill (Euphausia superba) is a key species of the marine Antarctic ecosystem. It is therefore crucial to understand how increasing water temperatures affect important krill life-cycle processes. Here, a long-term (August - March) laboratory acclimation experiment at different temperature scenarios (0.5 °C, 1.5 °C, 2.5 °C, 3.5 °C, 5 °C, 7 °C) was performed and the effects of elevated temperatures on whole animal parameters (O2 consumption, body length, length of the digestive gland) were analyzed. The response of krill oxygen consumption to different experimental temperatures differed between acute/short-term and long-term acclimation. After 8 months, krill oxygen consumption remained unchanged up to temperatures of 3.5 °C and was significantly higher at temperatures > 3.5 °C. Krill acclimated to temperatures ≥ 3.5 °C were significantly smaller at the end of the experiment. Limited food intake and/or conversion may have contributed to this effect, especially pronounced after the onset of the reproductive period. In addition, the seasonal growth pattern in males differed from that of females. Together, our findings indicate that warming Southern Ocean waters are likely to increase metabolic rate in krill, possibly altering the amount of energy available for other important life-cycle processes, a finding directly related to future population dynamics and fisheries management.

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.

Wintertime overlaps between female Antarctic fur seals (Arctocephalus gazella) and the krill fishery at South Georgia, South Atlantic.

The diet of Antarctic fur seals (Arctocephalus gazella) at South Georgia is dominated by Antarctic krill (Euphausia superba). During the breeding season, foraging trips by lactating female fur seals are constrained by their need to return to land to provision their pups. Post-breeding, seals disperse in order to feed and recover condition; estimates indicate c.70% of females remain near to South Georgia, whilst others head west towards the Patagonian Shelf or south to the ice-edge. The krill fishery at South Georgia operates only during the winter, providing the potential for fur seal: fishery interaction during these months. Here we use available winter (May to September) tracking data from Platform Terminal Transmitter (PTT) tags deployed on female fur seals at Bird Island, South Georgia. We develop habitat models describing their distribution during the winters of 1999 and 2003 with the aim of visualising and quantifying the degree of spatial overlap between female fur seals and krill harvesting in South Georgia waters. We show that spatial distribution of fur seals around South Georgia is extensive, and that the krill fishery overlaps with small, highly localised areas of available fur seal habitat. From these findings we discuss the implications for management, and future work.

A global population assessment of the Chinstrap penguin (Pygoscelis antarctica).

Using satellite imagery, drone imagery, and ground counts, we have assembled the first comprehensive global population assessment of Chinstrap penguins (Pygoscelis antarctica) at 3.42 (95th-percentile CI: [2.98, 4.00]) million breeding pairs across 375 extant colonies. Twenty-three previously known Chinstrap penguin colonies are found to be absent or extirpated. We identify five new colonies, and 21 additional colonies previously unreported and likely missed by previous surveys. Limited or imprecise historical data prohibit our assessment of population change at 35% of all Chinstrap penguin colonies. Of colonies for which a comparison can be made to historical counts in the 1980s, 45% have probably or certainly declined and 18% have probably or certainly increased. Several large colonies in the South Sandwich Islands, where conditions apparently remain favorable for Chinstrap penguins, cannot be assessed against a historical benchmark. Our population assessment provides a detailed baseline for quantifying future changes in Chinstrap penguin abundance, sheds new light on the environmental drivers of Chinstrap penguin population dynamics in Antarctica, and contributes to ongoing monitoring and conservation efforts at a time of climate change and concerns over declining krill abundance in the Southern Ocean.

Continuous moulting by Antarctic krill drives major pulses of carbon export in the north Scotia Sea, Southern Ocean.

Antarctic krill play an important role in biogeochemical cycles and can potentially generate high-particulate organic carbon (POC) fluxes to the deep ocean. They also have an unusual trait of moulting continuously throughout their life-cycle. We determine the krill seasonal contribution to POC flux in terms of faecal pellets (FP), exuviae and carcasses from sediment trap samples collected in the Southern Ocean. We found that krill moulting generated an exuviae flux of similar order to that of FP, together accounting for 87% of an annual POC flux (22.8 g m-2 y-1). Using an inverse modelling approach, we determined the krill population size necessary to generate this flux peaked at 261 g m-2. This study shows the important role of krill exuviae as a vector for POC flux. Since krill moulting cycle depends on temperature, our results highlight the sensitivity of POC flux to rapid regional environmental change.

Oxygen-dependence of upper thermal limits in crustaceans from different thermal habitats.

The critical thermal maximum (CTMAX) is the temperature at which animals exhibit loss of motor response because of a temperature-induced collapse of vital physiological systems. A central mechanism hypothesised to underlie the CTMAX of water-breathing ectotherms is insufficient tissue oxygen supply for vital maintenance functions because of a temperature-induced collapse of the cardiorespiratory system. The CTMAX of species conforming to this hypothesis should decrease with declining water oxygen tension (PO2) because they have oxygen-dependent upper thermal limits. However, recent studies have identified a number of fishes and crustaceans with oxygen-independent upper thermal limits, their CTMAX unchanged in progressive aquatic hypoxia. The previous studies, which were performed separately on cold-water, temperate and tropical species, suggest the oxygen-dependence of upper thermal limits and the acute thermal sensitivity of the cardiorespiratory system increases with decreasing habitat temperature. Here we directly test this hypothesis by assessing the oxygen-dependence of CTMAX in the polar Antarctic krill (Euphausia superba), as well as the temperate Baltic prawn (Palaemon adspersus) and brown shrimp (Crangon crangon). We found that P. adspersus and C. crangon maintain CTMAX in progressive hypoxia down to 40 mmHg, and that only E. superba have oxygen-dependent upper thermal limits at normoxia. In E. superba, the observed decline in CTMAX with water PO2 is further supported by heart-rate measurements showing a plateauing, and subsequent decline and collapse of heart performance at CTMAX. Our results support the hypothesis that the oxygen-dependence of upper thermal limits in water-breathing ectotherms and the acute thermal sensitivity of their cardiorespiratory system increases with decreasing habitat temperature.

Circadian regulation of diel vertical migration (DVM) and metabolism in Antarctic krill Euphausia superba.

Antarctic krill (Euphausia superba) are high latitude pelagic organisms which play a key ecological role in the ecosystem of the Southern Ocean. To synchronize their daily and seasonal life-traits with their highly rhythmic environment, krill rely on the implementation of rhythmic strategies which might be regulated by a circadian clock. A recent analysis of krill circadian transcriptome revealed that their clock might be characterized by an endogenous free-running period of about 12-15 h. Using krill exposed to simulated light/dark cycles (LD) and constant darkness (DD), we investigated the circadian regulation of krill diel vertical migration (DVM) and oxygen consumption, together with daily patterns of clock gene expression in brain and eyestalk tissue. In LD, we found clear 24 h rhythms of DVM and oxygen consumption, suggesting a synchronization with photoperiod. In DD, the DVM rhythm shifted to a 12 h period, while the peak of oxygen consumption displayed a temporal advance during the subjective light phase. This suggested that in free-running conditions the periodicity of these clock-regulated output functions might reflect the shortening of the endogenous period observed at the transcriptional level. Moreover, differences in the expression patterns of clock gene in brain and eyestalk, in LD and DD, suggested the presence in krill of a multiple oscillator system. Evidence of short periodicities in krill behavior and physiology further supports the hypothesis that a short endogenous period might represent a circadian adaption to cope with extreme seasonal photoperiodic variability at high latitude.

Relationship of morphometrics, total carotenoids, and total lipids with activity and sexual and spatial features in Euphausia superba.

Morphological differences associated with sex or stage, together with total lipids and carotenoids, were studied in Euphausia superba as possible indicators of physiological condition. E. superba displays sexual dimorphism during growth. A group of mature males, called Males II herein, has a greater abdominal length, suggesting that they are faster swimmers, a feature implying higher metabolic rates and a higher demand for protecting pigments like carotenoids. Mature Males II have proportionally lower lipids but higher total lipid-soluble carotenoids, a counterintuitive finding. Males II also have bigger eyes. Significant regressions with carotenoids were found for wet weight, abdominal length, and eye diameter. On a spatial analysis, population composition reflects reproductive activity. Males II would be in search of females for fecundation and, thus, are dominant in some areas. The PCA analysis of 10 allometric and biochemical variables show a distinct Males II group differing in morphology, carotenoids, and lipid contents. The carotenoid:lipid ratio was highest for Males II, supporting the hypothesis of the role of carotenoids in the activity of the species. Mature males may experience physiological stress during reproduction and probably die shortly afterwards. A relationship between activity, morphometrics, and carotenoid content seems evident, deserving further investigation.