The importance of Antarctic krill in biogeochemical cycles

Abstract

Antarctic krill (Euphausia superba) are swarming, oceanic crustaceans, up to two inches long, and best known as prey for whales and penguins - but they have another important role. With their large size, high biomass and daily vertical migrations they transport and transform essential nutrients, stimulate primary productivity and influence the carbon sink. Antarctic krill are also fished by the Southern Ocean's largest fishery. Yet how krill fishing impacts nutrient fertilisation and the carbon sink in the Southern Ocean is poorly understood. Our synthesis shows fishery management should consider the influential biogeochemical role of both adult and larval Antarctic krill.

Fig. 1

Processes in the biological pump. Phytoplankton convert CO₂, which has dissolved from the atmosphere into the surface oceans (90 Gt yr⁻¹) into particulate organic carbon (POC) during primary production (~ 50 Gt C yr⁻¹). Phytoplankton are then consumed by krill and small zooplankton grazers, which in turn are preyed upon by higher trophic levels. Any unconsumed phytoplankton form aggregates, and along with zooplankton faecal pellets, sink rapidly and are exported out of the mixed layer (< 12 Gt C yr⁻¹ ). Krill, zooplankton and microbes intercept phytoplankton in the surface ocean and sinking detrital particles at depth, consuming and respiring this POC to CO₂ (dissolved inorganic carbon, DIC), such that only a small proportion of surface-produced carbon sinks to the deep ocean (i.e., depths > 1000 m). As krill and smaller zooplankton feed, they also physically fragment particles into small, slower- or non-sinking pieces (via sloppy feeding, coprorhexy if fragmenting faeces), retarding POC export. This releases dissolved organic carbon (DOC) either directly from cells or indirectly via bacterial solubilisation (yellow circle around DOC). Bacteria can then remineralise the DOC to DIC (CO₂, microbial gardening). Diel vertically migrating krill, smaller zooplankton and fish can actively transport carbon to depth by consuming POC in the surface layer at night, and metabolising it at their daytime, mesopelagic residence depths. Depending on species life history, active transport may occur on a seasonal basis as well. Numbers given are carbon fluxes (Gt C yr⁻¹) in white boxes and carbon masses (Gt C) in dark boxes

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)

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 CO₂ drawdown. Some adult krill permanently reside deeper in the water column, consuming organic material at depth (8). Any carbon (as organic matter or as CO₂) 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 CO₂ 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 CO₂ 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

Fig. 4

Map of Antarctica and fishing areas for E. superba. Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR) Area 48 is subdivided into six smaller areas (48.1–48.6) covering the Atlantic sector of the Southern Ocean. Numbers in grey are subareas not fished and those in black are fished. Bathymetry is shown in blue with dark blue, representing deeper waters (data from the GEBCO_2014 Grid, version 20150318, http://www.gebco.net). The Antarctic coastline was obtained from the Scientific Committee on Antarctic Research (SCAR) Antarctic Digital Database

Fig. 5

Future research priorities on E. superba processes for the next decade. The pyramid illustrates the rates and states of krill life history, habitat and biogeochemical function, which need to be prioritised as areas of key research in the coming decade. The underlying ones, namely biomass (including spatial and temporal variations) and the residence depth of krill, are listed at the top of the pyramid. Determining the influence of climate change on all of these processes is vital. Autonomous vehicles fitted with biogeochemical sensors and cameras and acoustics will be instrumental in collecting data on this cryptic species. These key areas of research are needed to be able to parameterise krill in both ecosystem and biogeochemical models