Krill

Krill are shrimp-like marine invertebrate animals. These small crustaceans are important organisms of the zooplankton, particularly as food for baleen whales, mantas, whale sharks, crabeater seals and other seals, and a few seabird species that feed almost exclusively on them. Another name is euphausiids, after their taxonomic order Euphausiacea. The name krill comes from the Norwegian word krill meaning "young fry of fish".

Krill occur in all oceans of the world. They are considered keystone species near the bottom of the food chain because they feed on phytoplankton and to a lesser extent zooplankton, converting these into a form suitable for many larger animals for whom krill makes up the largest part of their diet. In the Southern Ocean, one species, the Antarctic Krill, Euphausia superba, makes up a biomass of over 500 million tons, roughly twice that of humans. Of this, over half is eaten by whales, seals, penguins, squid and fish each year, and replaced by growth and reproduction. Most krill species display large daily vertical migrations, thus feeding predators near the surface at night and in deeper waters during the day.

Commercial fishing of krill is done in the Southern Ocean and in the waters around Japan. The total global production amounts to 150–200,000 tonnes annually, most of this from the Scotia Sea. Most krill is used for aquaculture and aquarium feeds, as bait in sport fishing, or in the pharmaceutical industry. In Japan and Russia, krill is also used for human consumption and known as okiami (オキアミ) in Japan.

Taxonomy
The order Euphausiacea is split into two families. The family Bentheuphausiidae has only one species, Bentheuphausia amblyops, a bathypelagic krill living in deep waters below 1,000 m. It is considered the most primitive living species of all krill. The other family — the Euphausiidae — contains ten different genera with a total of 85 species. Of these, the genus Euphausia is the largest, with 31 species.

Well-known species — mainly because they are subject to commercial krill fishery — include Antarctic krill (Euphausia superba), Pacific krill (Euphausia pacifica) and Northern krill (Meganyctiphanes norvegica).

Distribution
Krill occur worldwide in all oceans; most species have transoceanic distribution and several species have endemic or neritic restricted distribution. Species of the genus Thysanoessa occur in both the Atlantic and the Pacific Ocean, which is also home to Euphausia pacifica. Northern krill occurs across the Atlantic, from the north to the Mediterranean Sea. The four species of the genus Nyctiphanes are highly abundant along the upwelling regions of the California, Humbolt, Benguela, and Canarias Current Systems, where occur most of the largest fisheries' activities of fish, molluscs and crustaceans.

In the Antarctic, seven species are known: one of the genus Thysanoessa (T. macrura) and six species of the genus Euphausia. The Antarctic krill (Euphausia superba) commonly lives at depths up to 100 m, whereas Ice krill (Euphausia crystallorophias) has been recorded at a depth of 4,000 m but commonly lives in depths at most 300 to 600 m deep. Both are found at latitudes south of 55° S; with E. crystallorophias dominating south of 74° S and in regions of pack ice. Other species known in the Southern Ocean are E. frigida, E. longirostris, E. triacantha, and E. vallentini.

Anatomy and morphology
Krill are crustaceans and have a chitinous exoskeleton made up of three segments: the cephalon (head), thorax, and the abdomen. The first two segments are fused into one segment, the cephalothorax. This outer shell of krill is transparent in most species. Krill feature intricate compound eyes; some species can adapt to different lighting conditions through the use of screening pigments. They have two antennae and several pairs of thoracic legs called pereiopods or thoracopods (so named because they are attached to the thorax; their number varies among genera and species). These thoracic legs include the feeding legs and the grooming legs. Additionally all species have five swimming legs called pleopods or "swimmerets," very similar to those of the common freshwater lobster. Most krill are about 1 to 2 cm long as adults, a few species grow to sizes of the order of 6 to 15 cm. The largest krill species is the mesopelagic Thysanopoda spinicauda. Krill can be easily distinguished from other crustaceans such as true shrimps by their externally visible gills.

Many krill are filter feeders: their front-most extremities, the thoracopods, form very fine combs with which they can filter out their food from the water. These filters can be very fine indeed in those species (such as Euphausia spp.) that feed primarily on phytoplankton, in particular on diatoms, which are unicellular algae. However, it is believed that all krill species are mostly omnivorous and some few species are carnivorous preying on small zooplankton and fish larvae.

Except for the Bentheuphausia amblyops species, krill are bioluminescent animals having organs called photophores that are able to emit light. The light is generated by an enzyme-catalyzed chemiluminescence reaction, wherein a luciferin (a kind of pigment) is activated by a luciferase enzyme. Studies indicate that the luciferin of many krill species is a fluorescent tetrapyrrole similar but not identical to dinoflagellate luciferin and that the krill probably do not produce this substance themselves but acquire it as part of their diet that contains dinoflagellates. Krill photophores are complex organs with lenses and focusing abilities, and they can be rotated by muscles. The precise function of these organs is as yet unknown; they might have a purpose in mating, social interaction or in orientation. Some researchers (e.g. Lindsay & Latz or Johnsen ) have proposed that krill use the light as a form of counter-illumination camouflage to compensate their shadow against the ambient light from above to make themselves more difficult to be seen by predators from below.

Behaviour
Most krill are swarming animals; the size and density of such swarms vary greatly depending on the species and the region. Of Euphausia superba, there have been reports of swarms of up to 10,000 to 30,000 individuals per cubic meter. Swarming is a defensive mechanism, confusing smaller predators that would like to pick out single individuals.

Krill typically follow a diurnal vertical migration. They spend the day at greater depths and rise during the night towards the surface. The deeper they go, the more they reduce their activity, apparently to reduce encounters with predators and to conserve energy. Some species (e.g. Euphausia superba, E. pacifica, E. hanseni, Pseudeuphausia latifrons, or Thysanoessa spinifera) also form surface swarms during the day for feeding and reproductive purposes even though such behaviour is dangerous because it makes them extremely vulnerable to predators.

Dense swarms may elicit a feeding frenzy among predators such as fish or birds, especially near the surface, where escape possibilities for the krill are limited. When disturbed, a swarm scatters, and some individuals have even been observed to molt instantaneously, leaving the exuvia behind as a decoy.

Krill normally swim at pace of a few centimetres per second (0.2–10 body lengths per second ), using their swimmerets for propulsion. Their larger migrations are subject to the currents in the ocean. When in danger, they show an escape reaction called lobstering: flipping their caudal appendages, i.e. the telson and uropods, they move backwards through the water relatively quickly, achieving speeds in the range of 10 to 27 body lengths per second, which for large krill such as E. superba means around 0.8 m/s. Their swimming performance has led many researchers to classify adult krill as micro-nektonic lifeforms, i.e. small animals capable of individual motion against (weak) currents. Larval forms of krill are generally considered zooplankton.

Ecology and life history
Krill are an important element of the food chain. Antarctic krill feed directly on phytoplankton, converting the primary production energy into a form suitable for consumption by larger animals that cannot feed directly on the minuscule algae, but that can feed upon krill. Some species like the Northern krill have a smaller feeding basket and hunt for copepods and larger zooplankton. Many other animals feed on krill, ranging from smaller animals like fish or penguins to larger ones like seal and even baleen whales.

Disturbances of an ecosystem resulting in a decline of the krill population can have far-reaching effects. During a coccolithophore bloom in the Bering Sea in 1998, for instance, the diatom concentration dropped in the affected area. However, krill cannot feed on the smaller coccolithophores, and consequently, the krill population (mainly E. pacifica) in that region declined sharply. This in turn affected other species: the shearwater population dropped, and the incident was even thought to have been a reason for salmon not returning to the rivers of western Alaska in that season.

Other factors besides predators and food availability also can influence the mortality rate in krill populations. There are several single-celled endoparasitoidic ciliates of the genus Collinia that can infect different species of krill and cause mass dying in affected populations. Such diseases have been reported for Thysanoessa inermis in the Bering Sea, but also for E. pacifica, Thysanoessa spinifera, and T. gregaria off the North-American Pacific coast. There are also some ectoparasites of the family Dajidae (epicaridean isopods) that afflict krill (and also shrimps and mysids); one such parasite is Oculophryxus bicaulis which has been found on the krill Stylocheiron affine and S. longicorne. It attaches itself to the eyestalk of the animal and sucks blood from its head; it is believed that it inhibits the reproduction of its host as none of the afflicted animals found reached maturity.

See also: Carbon sequestration, biological pump.

Life history
The general life-cycle of krill has been the subject of several studies (e.g. Guerny 1942, or Mauchline & Fisher 1969 ) performed on a variety of species and is thus relatively well understood, although there are minor variations in details from species to species. When krill hatch from the eggs, they go through several larval stages called the nauplius, pseudometanauplius, metanauplius, calyptopsis, and furcilia stages, each of which is sub-divided into several sub-stages. The pseudometanauplius stage is exclusive of species that lay their eggs within an ovigerous sac (so-called sac-spawners). The larvae grow and molt multiple times during this process, shedding their rigid exoskeleton and growing a new one whenever it becomes too small. Smaller animals molt more frequently than larger ones. Until and including the metanauplius stage, the larvae nourish on yolk reserves within their body. Only by the calyptopsis stages, differentiation has progressed far enough for them to develop a mouth and a digestive tract, and they begin to feed upon phytoplankton. By that time, the larvae must have reached the photic zone, the upper layers of the ocean where algae flourish, for their yolk reserves are exhausted by then and they would starve otherwise. During the furcilia stages, segments with pairs of swimmerets are added, beginning at the frontmost segments. Each new pair becomes functional only at the next molt. The number of segments added during any one of the furcilia stages may vary even within one species depending on environmental conditions.

After the final furcilia stage, the krill emerges in a shape similar to an adult, but is still immature. During the mating season, which varies depending on the species and the climate, the male deposits a sperm package at the genital opening (named thelycum) of the female. The females can carry several thousand eggs in their ovary, which may then account for as much as one third of the animal's body mass. Krill can have multiple broods in one season, with interbrood periods of the order of days.

There are two types of spawning mechanisms. The 57 species of the genera Bentheuphausia, Euphausia, Meganyctiphanes, Thysanoessa, and Thysanopoda are "broadcast spawners": the female eventually just releases the fertilized eggs into the water, where they usually sink into deeper waters, disperse, and are on their own. These species generally hatch in the nauplius 1 stage, but recently have been discovered to hatch sometimes as metanauplius or even as calyptopis stages. The remaining 29 species of the other genera are "sac spawners", where the female carries the eggs with her attached to its rearmost pairs of thoracopods until they hatch as metanauplii, although some species like Nematoscelis difficilis may hatch as nauplius or pseudometanauplius.

Some high latitude species of krill can live up to more than six years (e.g. Euphausia superba); others, such as the as mid-latitude species Euphausia pacifica, live only for two years. Subtropical or tropical species' longevity is still smaller, like e.g. Nyctiphanes simplex that usually lives only for six to eight months.

Molting occurs whenever the animal outgrows its rigid exoskeleton. Young animals, growing faster, therefore molt more often than older and larger ones. The frequency of molting varies wildly from species to species and is, even within one species, subject to many external factors such as the latitude, the water temperature, or the availability of food. The subtropical species Nyctiphanes simplex, for instance, has an overall intermolt period in the range of two to seven days: larvae molt on the average every three days, while juveniles and adults do so on the average every five days. For E. superba in the Antarctic sea, intermolt periods ranging between 9 and 28 days depending on the temperature between -1°C to 4 °C have been observed, and for Meganyctiphanes norvegica in the North Sea the intermolt periods range also from 9 and 28 days but at temperatures between 2.5 °C to 15 °C. E. superba is known to be able to reduce its body size when there is not enough food available, molting also when its exoskeleton becomes too large. Similar shrinkage has also been observed for E. pacifica (a species occurring in the Pacific Ocean from polar to temperate zones) as an adaptation to abnormally high water temperatures, and has been postulated for other temperate species of krill, too.

Economy
Krill has been harvested as a food source for humans (okiami) and domesticated animals since the 19th century, in Japan maybe even earlier. Large-scale fishing developed only in the late 1960s and early 1970s, and now occurs only in Antarctic waters and in the seas around Japan. Historically, the largest krill fishery nations were Japan and the Soviet Union, or, after the latter's dissolution, Russia and Ukraine. A peak in krill harvest had been reached in 1983 with more than 528,000 tonnes in the Southern Ocean alone (of which the Soviet Union produced 93%). In 1993, two events led to a drastic decline in krill production: first, Russia abandoned its operations, and second, the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR) defined maximum catch quotas for a sustainable exploitation of Antarctic krill. Nowadays, the largest krill fishing nations in the Antarctic are Japan, followed by South Korea, Ukraine, and Poland. The annual catch in Antarctic waters seems to have stabilized around 100,000 tonnes of krill, which is roughly one fiftieth of the CCAMLR catch quota. The main limiting factor is probably the high cost associated with Antarctic operations. The fishery around Japan appears to have saturated at some 70,000 tonnes.

Experimental small-scale harvesting is being carried out in other areas, too, e.g. fishing for Euphausia pacifica off British Columbia or harvesting Meganyctiphanes norvegica, Thysanoessa raschii and Thysanoessa inermis in the Gulf of St. Lawrence. These experimental operations produce only a few hundred tonnes of krill per year. Nicol & Foster consider it unlikely that any new large-scale harvesting operations in these areas will be started due to the opposition from local fishing industries and conservation groups.

Krill tastes salty and somewhat stronger than shrimp. For mass-consumption and commercially prepared products, they must be peeled because their exoskeleton contains fluorides, which are toxic in high concentrations. Excessive intake of okiami may cause diarrhea.