Carbon

Pelagic crustaceans such as krill can have a prominent role in regulating the magnitude of carbon stored in the ocean via the biological pump (Fig. 1)7,25. During photosynthesis, unicellular phytoplankton transform dissolved inorganic carbon (DIC or CO 2 ), a portion of which originates from the atmosphere, into organic carbon in their cells in the surface ocean26 (Fig. 1). Krill feed either directly on phytoplankton, or on protists and invertebrates (mainly zooplankton) that have consumed phytoplankton. A large part of the ingested carbon is absorbed (estimates range from 42 to 94%, dependent on food type and availability27), with the remainder being egested via their faecal pellets (Fig. 2). The absorbed carbon components are either catabolised to supply energy (leading to the respiration of CO 2 ), excreted as dissolved organic carbon28 or incorporated into body tissue and potentially transferred to krill predators.

Fig. 2 Cycling of nutrients by an individual krill. When krill moult they release dissolved calcium, fluoride and phosphorous from the exoskeleton (1). The chitin (organic material) that forms the exoskeleton contributes to organic particle flux sinking to the deep ocean. Krill respire a portion of the energy derived from consuming phytoplankton or other animals as carbon dioxide (2), when swimming from mid/deep waters to the surface in large swarms krill mix water, which potentially brings nutrients to nutrient-poor surface waters (3), ammonium and phosphate is released from the gills and when excreting, along with dissolved organic carbon, nitrogen (e.g., urea) and phosphorous (DOC, DON and DOP, 2 & 4). Krill release fast-sinking faecal pellets containing particulate organic carbon, nitrogen and phosphorous (POC, PON and POP) and iron, the latter of which is bioavailable when leached into surrounding waters along with DOC, DON and DOP (5) Full size image

Faecal pellets are an integral part of the biological pump8 (Fig. 1), with some being dense, compact particles that can sink quickly through the ocean. As krill are some of the largest pelagic crustaceans, they produce large faecal pellets (typically up to 1 cm length strings) with variable but often rapid sinking rates27,29. Krill pellets constitute the majority of sinking particles analysed in shallow (170 m) and deep (1500 m) Southern Ocean sediment traps deployed west of the Antarctic Peninsula and downstream of South Georgia respectively30,31. As krill mostly swarm in vast numbers, their contribution to particulate organic carbon flux can be huge, and estimates span over orders of magnitudes from 7 to 1300 mg C m−2 d−132,33,34,35. However, most observed rates tend to be at the lower end of that range, such as those reported in the marginal ice zone (e.g., 7–104 mg C m−2 d−1 at 100 m35). For reference, values of total (all particle types) particulate organic carbon flux in the Southern Ocean at 100 m, as determined by Thorium-234, ranges from 10 to 600 mg C m−2 d−1, with an average across latitudes between 100 and 150 mg C m−2 d−1 36. In the Scotia Sea (Atlantic Southern Ocean) where krill biomass is high18, total particulate organic flux at 100 m in the summer is up to 90 mg C m−2 d−1, with highest fluxes in the marginal/seasonal ice zones37. In the marginal ice zone over the productive season, the modelled estimate of the total export flux of krill faecal pellets at 100 m is 0.04 Gt C yr−135 (equivalent to 42 mg C m−2 d−1 based on the mean area of the marginal ice zone).

The number of faecal pellets observed generally declines with depth owing to scavenging and degradation5,6,38 (Fig. 3). However, some studies in the seasonal and marginal ice zones of the Southern Ocean indicate that krill faecal pellets can be transferred extremely efficiently, with minimal attenuation with depth, i.e., the amount of krill faecal pellet carbon in the surface is similar to that at depths of 100 s of metres below6,37,39. Such low rates of faecal flux attenuation have not been observed in other oceanic regions or for other crustaceans, suggesting that krill play a disproportionately important role in the sinking of carbon to the deep ocean35. Low attenuation of krill pellets in ice regions is likely owing to a combination of krill behaviour including pronounced vertical migrations37,39,40 and the formation of large swarms that produce a ‘rain’ of fast-sinking faecal pellets that overwhelm detrital consumers6,27,35,37,39. In addition, short migrations (40 m) just below the mixed layer can occur multiple times during a night’s feed, dependent on the satiation state of the krill41,42, which may increase the chance of faecal pellet export by shunting pellets deeper into the water column.

Fig. 3 Role of E. superba in biogeochemical cycles. Krill (as swarms and individuals) feed on phytoplankton at the surface (1) leaving only a proportion to sink as phytodetrital aggregates (2), which are broken up easily and may not sink below the permanent thermocline. Krill also release faecal pellets (3) whilst they feed, which can sink to the deep sea but can be consumed (coprophagy) and degraded as they descend (4) by krill, bacteria and zooplankton. In the marginal ice zone, faecal pellet flux can reach greater depths (5). Krill also release moults, which sink and contribute to the carbon flux (6). Nutrients are released by krill during sloppy feeding, excretion and egestion, such as iron and ammonium (7, see Fig. 2 for other nutrients released), and if they are released near the surface can stimulate phytoplankton production and further atmospheric CO 2 drawdown. Some adult krill permanently reside deeper in the water column, consuming organic material at depth (8). Any carbon (as organic matter or as CO 2 ) that sinks below the permanent thermocline is removed from subjection to seasonal mixing and will remain stored in the deep ocean for at least a year (9). The swimming motions of migrating adult krill that migrate can mix nutrient-rich water from the deep (10), further stimulating primary production. Other adult krill forage on the seafloor, releasing respired CO 2 at depth and may be consumed by demersal predators (11). Larval krill, which in the Southern Ocean reside under the sea ice, undergo extensive diurnal vertical migration (12), potentially transferring CO 2 below the permanent thermocline. Krill are consumed by many predators including baleen whales (13), leading to storage of some of the krill carbon as biomass for decades before the whale dies, sinks to the seafloor and is consumed by deep sea organisms Full size image

Vertical migrations can also shunt carbon to depth when krill occupy deeper layers and respire carbon consumed at the surface, a process termed active carbon flux. This occurs especially in younger developmental stages of E. superba (larvae and juveniles), which can undergo extensive diel (daily) vertical migrations (DVMs)43,44 travelling to deeper depths than adults, often below permanent thermoclines41,45 (Fig. 3). Larval DVMs may follow a normal pattern of ascent during the night and descent during the day46, or a reverse pattern of ascent during the day and descent at night44. DVM patterns in adult krill are less clear, and a range of behaviours may be exhibited, including normal and reverse DVM as well as remaining at particular depths throughout the diel cycle47,48, so their biogeochemical role may differ depending on the depth they inhabit or migrate to. Even so, where DVM does take place in adults, they generally remain above the permanent thermocline, within the surface mixed layer49. Difficulties in resolving the complex DVM of Antarctic krill means that estimates of the total contribution of this species to active carbon flux have yet to be fully resolved41,48,50.

There are further additional mechanisms by which krill might contribute to the carbon sink. For instance, in winter adult E. superba populations appear to move to coastal basins51 and studies using under-water cameras and active acoustics have revealed that krill aggregate at greater depths in winter than in summer52,53. Metabolism of their lipid reserves to CO 2 when residing in deeper waters in winter, as observed in copepods54, releases surface-produced carbon to the deep ocean. This process is termed the lipid pump and is significant in that it moves carbon to depth without depleting surface concentrations of potentially limiting nutrients over winter (e.g., nitrogen and phosphorus). Rapid transport of carbon to the deep ocean/sea floor is also facilitated by the short phytoplankton-krill-whale food chain, where krill carbon is stored as biomass in baleen whales for decades, whose carcasses rapidly sink to the deep sea floor when they die55 (Fig. 3). Finally, some E. superba also feed on detritus on the seabed, often at great depth, and are then fed upon by benthic fish and invertebrates meaning the carbon stays in the deep ocean50 (Fig. 3). The contribution of all these processes to carbon transport is potentially significant but remains unquantified.

Iron

Iron is an important trace element in the oceans and its low availability limits primary productivity in large areas, including much of the ice-free Southern Ocean56,57. The largest sources of new iron to the Southern Ocean surface waters are deep winter mixing58 and the seasonal melting of sea ice59. Following the depletion of this winter-spring iron pulse, further primary production depends increasingly on recycled iron58. E. superba have an important role in oceanic iron cycling49,50,60,61,62 facilitated by the ingestion of iron-rich phytoplankton and lithogenic particles. The iron concentration in an individual whole adult krill ranges from 4.4 to 190.5 mg kg−149,50,60,61,63,64, with the > 40-fold difference in krill iron content reflecting seasonal and regional differences in their dietary iron content64. Eventually, the iron retained in individual bodies can be released back into surface waters when baleen whales and other vertebrates consume E. superba and subsequently defecate60. Thus, in the iron-limited Southern Ocean iron recycled via krill and their predators is important for stimulating primary production (Fig. 3).

A small proportion of dissolved iron (dFe, < 0.2 μm49) in excess of the demand by E. superba is excreted, with excretion rates ranging from 0.2 to 5.5 nmol dFe ind−1 d−149. Highest rates occur when krill feed on diatoms, which is consistent with some diatoms’ ability to acquire and store excess intracellular iron65. Upon digestion of phytoplankton, E. superba may also release iron-binding ligands (e.g., porphyrin compounds)9, which can complex with inorganic iron and thereby increase the concentration of soluble iron available to phytoplankton49. However, most (90%) of the iron in E. superba is released via their fast-sinking faecal pellets, which have 3–4 orders of magnitude more iron their muscle tissue (Fig. 2)49. Therefore, the cycling of iron via krill is closely linked to the fate of their faecal pellets, which may sink to great depths without being consumed37,39. A study on salps showed that iron was not readily leached from their faecal pellets66, and, if also true for krill, their pellets would need to be fragmented to release dFe into the water column as the pellet sinks. Nevertheless, the feeding activity of the abundant E. superba as a whole provides the basis for several pathways of dFe supply to phytoplankton (Fig. 3)—involving also microbes, zooplankton and krill predators—which, together with the release of ligands, can benefit phytoplankton growth. Such fertilising processes mediated by krill may explain why phytoplankton blooms downstream of the island of South Georgia last longer and are more intensive during years with high krill abundances on-shelf49.

Macronutrient regeneration and grazing

Krill also release macronutrients such as ammonium (Fig. 3), which can be particularly important in iron-limited regions, as using ammonium rather than nitrate reduces the phytoplankton iron demand by ~ 30 %67. Regions of frequently high but spatially variable E. superba density have been used as a series of natural experiments in examining the role of krill nutrient recycling and grazing in shaping the abundance and composition of phytoplankton. At South Georgia, grazing was sufficient to suppress phytoplankton biomass toward the east of the island68, yet E. superba ammonium excretion also supplied a large fraction of the requirements to the ungrazed cells. Rates of ammonia excretion in South Georgia have been measured to range from 12 to 273 nmol NH 4 ind−1 h−169, with higher rates measured further south off the Western Antarctic Peninsula (61–475 nmol NH 4 ind−1 h−1)70.

In addition, E. superba grazing and deep mixing has been found to shift the phytoplankton community from diatoms to flagellates at the Antarctic Peninsula71. Krill grazing can also fragment phytoplankton cells or other particulate matter releasing dissolved organic matter into the water (termed sloppy feeding, Figs. 1 & 2)38,72, which can be further broken down and remineralised by bacteria (termed microbial gardening73). This process reduces the flux of carbon to the deep ocean, although, thus far a link between sloppy feeding and increased microbial activity has not been explicitly shown for krill. E. superba can thus exert two opposing top–down controls on phytoplankton; they can rapidly graze blooms decreasing phytoplankton biomass but also excrete nutrients increasing phytoplankton biomass.

Transport of nutrients

In addition to shunting carbon to deeper waters, krill are also involved in the vertical and lateral transport of other nutrients. For instance, adult E. superba moult as often as every 2 weeks depending on temperature and season74, resulting in a high number of moults produced per krill over their long life-span (5–6 years in wild). The release of moults, which sink at rates of 50–1000 m d−175, contributes to the carbon sink, but also to the release of other micronutrients to the water column as the moult sinks. For instance, fluoride concentrations in live E. superba exoskeletons are at least 2500 times higher than the surrounding waters76, and this fluoride is leached out during ecdysis75 and degradation of the exoskeletons. A range of other elements are also found in the exoskeletons of krill, for example the exoskeleton contains 47% of the phosphorous and 84% of the calcium concentrations of these minerals in krill77. How quickly these nutrients are released from shedded exoskeletons (moults) and their possible contribution to biogeochemical cycles has yet to be quantified.

Krill can also mix nutrients; mass migrations of krill swarms from deep nutrient-rich water, particularly in localised, permanently or temporarily oligotrophic waters, could mix nutrients to the surface and stimulate phytoplankton growth42,78 (Fig. 3). Conversely, the carbon transferred by krill from the surface to below the mixed layer is subjected to remineralisation by bacteria and detritivores, which convert dissolved organic carbon to CO 2 6,38. The depth at which this remineralisation occurs, or the depth of krill respiration, is crucial for determining the longevity of CO 2 storage in the deep ocean; i.e., whether the released CO 2 is mixed back up to the surface (shallow remineralisation) or is stored for decades in the deep ocean (deep remineralisation)79. If CO 2 is released above the permanent thermocline (deepest winter mixed layer depth, globally < 750 m80), then CO 2 will be subjected to seasonal physical mixing to the surface ocean and potentially re-exchanged with the atmosphere within a year following release from the krill (Fig. 3). The length of time CO 2 (or nutrients) will remain in the deep ocean also depends on the water mass it enters owing to ocean circulation81. For E. superba that live south of the Antarctic Circumpolar Current (ACC, i.e., a substantial part of the population82), any nutrients they release will likely remain in the Southern Ocean. However, nutrients released from an organism within the ACC, or at the northern boundary of the ACC, may be subducted into the Antarctic Intermediate Water. Currently we do not know whether nutrients released by Southern Ocean organisms make a significant contribution to production elsewhere.

Larval stages

The contribution of larval krill to biogeochemical cycles is different to that of adults due to their unique pattern of growth and development, smaller size and feeding ecology83. Larval E. superba use sea ice as a feeding ground and shelter84 and owing to their ingestion of ice biota and subsequent migration into the water column, play an important role in ice-pelagic coupling. E. superba larvae consume up to 26% of their body weight in carbon per day, of which ~ 10% is egested as faecal pellets85. This equates to larval egestion of ~ 4 µg C d−1, which is ~ 1000 times less than adults41 although in the Scotia Sea they can be up to 100 times more abundant than adults86. If these relative abundances hold across the wider ocean sector, this would equate to larvae contributing an additional 1–10% of the adult faecal pellet flux. Furthermore, DVM in larval E. superba takes them considerably deeper than adults (400 m and 200 m, respectively)43,48. The pronounced DVM patterns of larval krill in the proximity of ice may be responsible for the low attenuation of krill faecal pellets with depth in the marginal ice zone of the Atlantic Southern Ocean6,37 (Fig. 3), rather than the DVMs of adult krill. Larvae may be more likely to contribute to active transport of carbon via egestion and respiration at depth, although the mass and sinking potential of larval faecal pellets have yet to be characterised.

In summary, E. superba influence many biogeochemical cycles including carbon, nitrogen and iron, from larval through to adult life stages, and also have a diverse, multi-faceted role within these individual elemental cycles. Whilst there has been some focus on the contribution of E. superba to organic carbon and iron cycles, given our current lack of knowledge and uncertainty in biomass estimates, (Box 1) it is difficult to quantify its complete role in these cycles. Nonetheless, the substantial biomass, diurnal vertical migrations and broad horizontal distribution of E. superba suggests a significant contribution. Quantification of these rates, as well as better constrained estimates of krill biomass, are critical to provide meaningful data so biogeochemical modellers can sufficiently parameterise the influence of E. superba on nutrient cycles. A better understanding of krill–nutrient interactions will also allow assessment of the impact of human activities, particularly fishing, on biogeochemical cycles and help to identify management approaches that will minimise these impacts.