Krill evolution and the Antarctic ocean currents: evidence of vicariant speciation as inferred by molecular data

The phylogenetic relationships of the Antarctic krill Euphausia superba, the key species in the Antarctic food web, and other Antarctic and sub-Antarctic cuphausiids have been investigated using the 16S ribosomal mitochondrial gene. The phylogenetic reconstructions indicated that the Antarctic species form a monophyletic clade separated by the non-Antarctic species. The results revealed a large genetic divergence between the Antarctic (E. superba and E. crystallorophias) and sub-Antarctic species (E. vallentini). The time of separation between these species, estimated from the molecular data, is around 20 million years ago, which is comparable with the geological time of the formation of a circum-Antarctic water circulation and the Antarctic Polar Frontal Zone. The euphausiid molecular phylogeny therefore represents evidence for vicariant speciation.     

Lipid metabolism of the Antarctic krill Euphausia superba and its ecological implications

 Various developmental stages (early larvae to adults) of Euphausia superba have been collected in different seasons in the Weddell Sea, the Lazarev Sea and off the Antarctic Peninsula to investigate the role of lipids and fatty acids in the life cycle of the Antarctic krill. The total-lipid data for E. superba exhibited seasonal variations, with low lipid levels in late winter/early spring and the highest levels in autumn. Seasonal changes were most pronounced in the immature and adult specimens, increasing from about 10% lipid of dry mass to more than 40%. The fatty-acid compositions of the younger stages were dominated by 20:5(n-3), 22:6(n-3) and 16:0. These are typical phospholipid fatty acids, which are major biomembrane constituents. The phospholipid composition was similar in the older stages. With increasing storage of triacylglycerols in the lipid-rich immature and adult stages, the fatty acids 14:0, 16:0 and 18:1(n-9) prevailed, comprising about 70% of total triacylglycerol fatty acids. The trophic-marker fatty acids 16:1(n-7) and 18:4(n-3), indicating phytoplankton ingestion, were less abundant. They reflected, however, the dependence of the larvae on phytoplankton as well as the seasonal changes in algal composition. The generally close linear relationships between fatty acids and lipid suggest that the fatty-acid compositions of the collected specimens were largely independent of the respective developmental stage, season and region. The linear fit indicates that triacylglycerol accumulation started at a level of about 5% of total lipid. Considering the various overwintering scenarios under discussion, the life cycle and reproductive strategies of krill are discussed in the context of the lipid metabolism and fatty-acid composition of E. superba. Lipid production is effective enough to accumulate large energy reserves for the dark season, but E. superba does not exhibit the sophisticated biosynthetic pathways known from other Antarctic euphausiids and copepods. Although important, lipid utilisation appears to be just one of several strategies of E. superba to thrive under the extreme Antarctic conditions, and this pronounced versatility may explain the success of this species in the Southern Ocean. Received: 16 June 2000 / Accepted: 18 December 2000     

The fatty acids of antarctic phytoplankton and euphausiids. Fatty acid exchange among trophic levels of the Ross Sea

The fatty acids of 3 samples of Euphausia superba, 7 samples of E. crystallorophias, and 12 samples of phytoplankton collected in the Ross Sea, Antarctica, during Eltanin Cruise 51 were examined. The fatty acid profiles of the samples of E. superba resembled each other closely. The fatty acid profiles of the E. crystallorophias samples were also similar to each other but different quantitatively from those of E. superba. Phytoplankton fatty acid patterns varied with the geographical location and species composition of the samples. The fatty acids of euphausiids were compared to those of the phytoplankton from the corresponding locations. Rather similar fatty acid patterns in phytoplankton and E. superba corroborate the herbivorous nature of this euphausiid. On the other hand, phytoplankton and E. crystallorophias showed quite different fatty acid patterns. The differences were mostly due to the presence of waxes among the lipids of E. crystallorophias. It is not clear whether these waxes are of dietary origin or are synthesized endogenously.     

Fluoride in Antarctic marine crustaceans

The concentration of fluoride in the body parts of a range of Antarctic crustaceans from a variety of habits was examined with the aim of determining whether fluoride concentration is related to lifestyle or phylogenetic grouping. Euphausiids had the highest overall fluoride concentrations of a range of Antarctic marine crustaceans examined; levels of up to 5477 μg g⁻¹ were found in the exoskeleton of Euphausia crystallorophias. Copepods had the lowest fluoride levels (0.87 μg g⁻¹ whole-body); some amphipods and mysids also exhibited relatively high fluoride levels. There was no apparent relationship between the lifestyle of the crustaceans and their fluoride level; benthic and pelagic species exhibited both high and low fluoride levels. Fluoride was concentrated in the exoskeleton, but not evenly distributed through it; the exoskeleton of the head, carapace and abdomen contained the highest concentrations of fluoride, followed by the feeding basket and pleopods, and the eyes. The mouthparts of E.␣superba contained almost 13 000 μg F g⁻¹ dry wt. Antarctic krill tail muscle had low levels of fluoride. After long-term (1 to 5 yr) storage in formalin, fluoride was almost completely lost from whole euphausiids. Received: 1 April 1998 / Accepted: 29 July 1998     

Growth of Antarctic krill Euphausia superba at South Georgia

 Antarctic krill Euphausia superba has a central role in the ecosystem of the Southern Ocean and knowledge of its growth rate is central to determining the factors influencing population dynamics. The length of Antarctic krill in the diet of Antarctic fur seals Arctocephalus gazella at South Georgia revealed a consistent increase in size between ca. 42 and ca. 54 mm over the period October–March, indicating growth rates much higher than predicted by existing models. Geographical variation in growth rate may result in 2-year-old krill at South Georgia attaining the same size as 3-year-old krill in the Antarctic Peninsula region. The effect of geographical variation in growth rate on the population structure of krill has important implications for comparing the fate of individual cohorts over large scales and in the interpretation of krill life-cycles. Received: 20 May 2000 / Accepted: 11 August 2000     

Polonium-210 and lead-210 in Antarctic marine biota and sea water

Concentrations of the naturally-ocurring radionuclides ²¹⁰Po and ²¹⁰Pb were measured in krill (Euphausia superba), mesozooplankton, phytoplankton and sea water collected during the South African SIBEX cruise to the Antarctic in autumn 1984. The data reported constitute the first substantial measurements on ²¹⁰Po and ²¹⁰Pb in such samples in the Antarctic Ocean. The concentrations of ²¹⁰Po in mesozooplankton and phytoplankton are unexceptional in comparison with those from other oceans. The SIBEX E. superba, however, have higher levels of ²¹⁰Po than usually found in euphausiids. The ²¹⁰Po data, combined with reasonable estimates of biological quantitites such as the fractional assimilation, are used to obtain information about the diet of E. superba. It is suggested that the higher ²¹⁰Po in the SIBEX E. superba reflects a change from an almost entirely phytoplanktonic diet in summer to a more omnivorous diet as winter approaches. The data show that there are allometric relationships between the ²¹⁰Po content of euphausiids and animal size; these are discussed briefly. The limited sea-water data presented are characterized by unusually high ²¹⁰Po:²¹⁰Pb activity ratios and need further investigation.     

Potential for long-distance dispersal of Euphausia crystallorophias in fast current jets

The euphausiid Euphausia crystallorophias Holt and Tattersall, 1906 is considered to be a neritic species. It has been found in greatest abundance along the Antarctic continental margins, often in association with regions of pack ice. Although E. crystallorophias has been observed at some islands to the west of the Antarctic Peninsula, the species has not previously been reported from islands of the maritime- or sub-Antarctic further north. During an oceanographic transect in November 1997 from South Georgia to the South Sandwich Islands, acoustic observations revealed a dense, discrete pelagic target at 50 m. The target was fished and was found to be an aggregation of small E. crystallorophias. The fishing location (54.48°S; 30.61°W) was >1500 km from the Antarctic continent, and >250 km from the nearest land, in water of several thousands of metres depth – clearly a non-neritic environment. Examination of hydrographic data revealed that the E. crystallorophias swarm had been located within a fast-flowing band of water that had characteristics of water found near the Antarctic Peninsula. This band was ≃150 km wide, and had a speed ranging from 9 to 22 km d⁻¹ in a north-easterly direction. The possible origins of this E. crystallorophias swarm are explored in the light of the eddy-dominated current patterns prevalent in the Weddell–Scotia Confluence region, and with reference to published growth-rate estimates for the species. We discuss the potential for long-distance dispersal of E. crystallorophias and other neritic species in fast current jets, and examine how such oceanographic features could facilitate long-distance dispersal, colonization, and gene flow. Received: 23 November 1998 / Accepted: 25 March 1999     

Effect of temperature on the molting,growth and maturation of the antarctic krill Euphausia superba (Crustacea: Euphausiacea) under laboratory conditions

The effect of temperature on molting, growth, and maturation rates was studied on laboratory-maintained Euphausia superba. The length of intermolt periods (IMP's) was inversely proportional to temperature (20.10 d, SD=1.60, at 0.12°C; 16.87 d, SD=1.68, at 0.97°C; and 12.48 d, SD=0.90, at 4.48°C), and directly proportional to krill size at 0.12°C and 0.97°C. For individually maintained krill the maximum growth rate at 4.48°C (0.068 mm d^-1) was nearly twice that at 0.68°C (0.037 mm d^-1). There was no observable temperature effect on maturation rates. The maturation changes of juveniles at all temperatures indicated that more than two years are probably required to reach maturity. Mature males and females regressed to immature forms, suggesting that E. superba may reproduce in successive years. These results and previously reported field and laboratory data for E. superba and other euphausiid species suggest a 4+ year life span for this species.This work was supported by NSF grant DPP 76-23437     

Change in the gross biochemistry and mineral content accompanying the moult cycle in the Antarctic krill Euphausia superba

Concentrations of water, ash, protein, chitin, lipid, calcium, magnesium, sodium, potassium, strontium and copper were measured in individuals from a laboratory population of Antarctic krill, Euphausia superba Dana, over the course of a moult cycle. Significant changes in all variables were encountered. Total ash, lipid, calcium, magnesium and strontium all increased in concentration following moulting. Water, protein and copper concentrations all decreased following ecdysis and increased again towards the end of the moult cycle. The major ions sodium and potassium fluctuated around mean levels. Cast moults of E. superba were shown to be a drain on the ionic load of the krill, and the losses inherent in exuviation could account for much of the variation observed during the moult cycle.     

Reproductive trade-off in male Antarctic krill,Euphausia superba

Freshly caught male and female Euphausia superba from the same swarm exhibited different rates of mortality subsequent to capture. Mortality was significantly higher for reproductive males (100%, n=68) than for females (3%, n=186) within the first 3 d of capture. Total lipid and triacylglycerol levels in male, female and juvenile Euphausia superba were analysed and compared. All reproductive male krill analysed from this swarm had low lipid levels (1 to 3% dry weight) with negligible triacylglycerol stores (0 to 2% of total lipid). Somatic lipid stores in female and juvenile krill ranged from 8 to 30% of which up to 40% was triacylglycerol. The levels of algal sterols in the digestive gland of males, females and juveniles indicate that all krill had been feeding recently. An analysis of the sex ratio of krill catches derived from data collected over seven summers from the Prydz Bay region showed a decrease in the proportion of males with increasing size. There was a sharp decline in numbers of male krill once they attained a length of 51 to 55 mm. Low lipid levels in redroductive male krill may be due to reproductive costs. The resulting low storage-lipid levels are accompanied by high mortality in male krill.     

Larval distribution and reproductive ecology of Thysanoessa macrura (Crustacea: Euphausiacea) in the Scotia Sea

In the Scotia Sea, the larvae of Thysanoessa macrura G.O. Sars, 1885 were scarce in spring (September 27 to October 6, 1971) and mainly present at the Calyptopis I stage, while in summer (December 17, 1974 to January 3, 1975) they were much more abundant and much further developed (up to Furcilia VI). The spawning season commences as early as September and, as indicated by the presence of numerous nauplii and metanauplii in summer, is rather long. T. macrura begins to spawn much earlier in West-Wind-Drift waters than in waters of the Weddell Sea. It starts to spawn simultaneously with Euphausia frigida and E. triacantha, but significantly earlier than E. superba. These timings of the breeding process are related to differential biogeographical characteristics of these species. Plankton collections made at depths of 500 or 1000 m have, for T. macrura, revealed a developmental ascent analogous to that of E. superba. Ontogenetical deep-water migrations are, consequently, characteristic not only for E. superba, but also for other Antarctic euphausiids (in particular E. frigida, but possibly not for inshore E. crystallorophias) and, as correctly postulated by several other investigators, for all oceanic euphausiid species.     

Laboratory and field estimates of the rate of faecal pellet production by Antarctic krill,Euphausia superba

The time course of faecal pellet production (egestion) was monitored in January 1985 for a population of Antarctic krill, Euphausia superba Dana, maintained in flowing seawater aquaria at Palmer Station, Antarctica. Following transfer to filtered seawater, krill produced faecal strings for roughly 40 min, after which time faecal egestion virtually ceased. Similar results were obtained for freshly-trawled krill at sea in February and March 1985. There were wide daily variations in total faecal egestion rate; mean rates varied from 0.54 to 1.66 mg dry wt h^-1 and individual rates from 0.25 to 2.35 mg h^-1 (all data corrected to a standard krill of 600 mg fresh weight). Despite these wide fluctuations in total faecal egestion, the loss of organic matter showed no significant daily variation, with a mean value of 0.13 mgh^-1. The relationship between faecal egestion rate and faecal organic content suggested that feeding rate was governed by food quality; when inorganic load was high, feeding rate increased to ensure sufficient energy intake. The data suggest that superfluous feeding does not occur in krill and that values of gut-clearance time calculated from time intervals greater than about 40 min will not be representative of previous feeding history. the rates of faecal egestion observed in this study indicate that the flux of faecal pellets from krill is substantial. They imply an energy intake in E. superba of 17 to 28% body weight per day, much higher than estimated previously for this species by summing known energy losses, but similar to estimates for other euphausiids.     

Schooling behavior of Antarctic krill (Euphausia superba) in laboratory aquaria: Reactions to chemical and visual stimuli

Antarctic krill,Euphausia superba, often exhibit abnormal behavior in laboratory aquaria, usually hovering in a stationary position, unresponsive to most external stimuli. In the austral summer of 1985–1986 at Palmer Station on Anvers Island, Antarctica, we provided laboratory conditions which inducedE. superba to school in large aquaria. Captive krill swam horizontally and exhibited the full spectrum of behaviors normally displayed while schooling at sea. Schooling krill avoided visually contrasting stimuli, with avoidance distances correlated with stimulus size. Schools responded in qualitatively different ways to presentations of food, chemical compounds, and abrupt increases in light intensity. We describe the conditions necessary for aquarium schooling and discuss the importance of an appropriate social environment for displays of escape, avoidance, and feeding behaviors and of positional preference within the school.     

Metabolism and body composition of two euphausiids (Euphausia superba and E. crystallorophias) collected from under the pack-ice off Enderby Land,Antarctica

Oxygen consumption, ammonia excretion and phosphate excretion rates were measured for Euphausia superba and E. crystallorophias captured under the pack-ice off Enderby Land, Antarctica, during November 1985. Water, ash, carbon, nitrogen and phosphorus composition were also determined. Compared with summer data, body composition of E. superba at this time of year was characterized by low carbon (40.2 to 40.7% of total dry wt), high nitrogen (11.8 to 12.0%), high phosphorus (1.2%) and high water (80.6 to 81.7% of total wet wt) content. Metabolic rates, expressed as percentage daily losses of body carbon, nitrogen and phosphorus were 1.3 to 1.6%, 0.38 to 0.42% and 1.9 to 2.2%, respectively; these fall within the ranges of summer data. E. superba fed on algae growing on the bottom of the ice, but body compositional features of this species suggest limited contribution of ice-algae to nutrition. Compared to E. superba, E. crystallorophias displayed greater metabolic rates and much higher body carbon content (40.9 to 45.0%), implying that feeding conditions under the ice were better suited to the requirements of E. crystallorophias. The only gravid females found belonged to E. crystallorophias.     

Contribution of heterotrophic material to diet and energy budget of Antarctic krill, Euphausia superba

A novel approach was used to estimate the heterotrophic carbon component in the diet of the Antarctic krill Euphausia superba. Over 200 specimens from seven samples collected in the Lazarev Sea (January 1993 and 1995), at the Antarctic Polar Front (January 1993), and around South Georgia (February/March 1994) were dissected, and the total carbon content of their stomachs was estimated with a CHN-analyser. Gut-pigment contents were also measured by the gut-fluorescence technique in specimens collected at the same time, and the equivalent amount of their gut carbon was then subtracted from the total organic carbon content of guts from the same samples. The remaining carbon was assumed to originate entirely from heterotrophic food sources. This heterotrophic component accounted for a substantial proportion of the total food consumed by Antarctic krill, ranging from 17.4 to 98.9% of the mass of the gut contents (mean = 78.8% ± 21.2 SD). The results make an important contribution to the elucidation of the energy budget of krill and its daily carbon ration. With a few exceptions, previous estimates were largely calculated from a solely autotrophic carbon source, and were unable to account for the metabolic requirements of E. superba. Krill plays an important role in Antarctic food webs, as it often constitutes ≃50% of the total biomass of the zooplankton, and produces fast-sinking, dense faecal pellets which are important in the vertical transport of organic carbon from the euphotic layer to the deep ocean. High consumption rates of smaller heterotrophic organisms by krill suggest that this large microphage may be more important than previously believed in re-packaging micro- and mesozooplankton into a longer-lasting and more easily sequestered carbon pool. Received: 26 October 1998 / Accepted: 14 October 1999     

Using a high-powered strobe light to increase the catch of Antarctic krill

Adult euphausiids are difficult to capture with the nets typically used by oceanographers due in part to avoidance of the net. A cruise of the Southern Ocean GLOBEC program (NBP0103) in April/May 2001 permitted an evaluation of the efficacy of a high-powered strobe light (150 W) mounted on a 1-m² multiple opening/closing net and environmental sampling system (MOCNESS) in reducing net avoidance. Three horizontal tows were made in Laubeuf Fjord, Marguerite Bay (western Antarctic Peninsula, 67.89°S; 68.30 W) on 28–29 May in an area that had a high abundance of adult krill (mostly Euphausia superba, Dana and a few E. crystallorophias, Holt and Tattersall). Each tow consisted of a series of paired down and up casts through a set depth interval (e.g. 50–90 m), with each successive net (335 µm mesh) sampling both a down and up cast. The strobe light was either on or off while each net was open, and when on, the light flashed at 4-s intervals. During a tow, four of the eight nets sampled with the strobe flashing and four sampled with the strobe off, in a random sequence. Total zooplankton displacement volume was significantly higher (P<0.05), on average by a factor of ~1.5, when the strobe light was on. The increased biovolume was due to the enhanced catch (factor of ~2) of adult krill (15–60 mm length). There was no enhanced catch of smaller krill (5–15 mm length: a mixture of E. superba, E. crystallorophias, and Thysanoessa macrura, GO Sars). In addition, the average length of the large krill fraction was not changed substantially with the strobe light on. These results suggest that krill avoidance of nets can be overcome by intense strobe lighting.Electronic Supplementary Material Supplementary material is available in the online version of this article at http://dx.doi.org/10.1007/s00227-003-1228-z.Communicated by J.P. Grassle, New Brunswick     

Ecological implications of fecal pellets produced by the Antarctic krill Euphausia superba in the Antarctic Ocean

Organic analyses and electron microscopic observations on fecal pellets produced by the Antarctic krill Euphausia superba Dana showed that krill fed on choanoflagellates, the abundant heterotrophic flagellate in the Antarctic Ocean. Two new pathways of organic materials in the Antarctic ecosystem are proposed: (1) a new food chain including non-living particulate and dissolved organics, and bacteria-choanoflagellate-krill-vertebrate, which coexists with the traditional diatom-krill-vertebrate food chain; (2) non-phytoplanktonic organic materials in surface waters are transferred into choanoflagellates and are transported to deep water as fecal pellets which are still useful as nutrition for other organisms there.     

Layers of Antarctic krill, Euphausia superba : are they just long krill swarms?

Antarctic krill, Euphausia superba Dana, a major component in the southern ocean food web, typically occur in aggregations that range from small, discrete swarms and schools through to layers and superswarms that extend horizontally for several kilometres. A large Longhurst–Hardy plankton recorder has been used to obtain high-resolution serial samples from within two layers (up to 4 km in length) that were found near Elephant Island, north of the Antarctic Peninsula. Krill length, sex and maturity stage, net and acoustic estimates of number density are shown to vary significantly within these large layers. The variation occurring within a single layer is comparable with that occurring in a set of 38 swarms sampled contemporaneously with the layers. Thus, unlike a krill swarm, a whole krill layer may account for a substantial amount of the variation in the local krill population, although individual parts of the layer cannot be considered in this way. The layers play an important role in the ecology of the krill within the area. Firstly, these large layers may contain a significant proportion of the biomass within an area. Secondly, the structure of the layers gives some insight into the ways in which krill swarm formation and dispersal may be occurring. Received: 28 March 1997 / Accepted: 3 December 1997     

A universal method for quantifying and comparing the residual variability of element concentrations in biological tissues using 25 elements in the mussel Mytilus edulis as a model

Heavy metal concentrations (especially Cu, Cd and Zn) have been measured in oceanic hyperiid amphipods (Themisto gaudichaudii and T. compressa) and euphausiids (Meganyctiphanes norvegica and Euphausia superba), collected in the Antarctic and Atlantic Oceans. In some cases, metal concentrations displayed size-dependencies which were allowed for in interspecific or intersite comparisons, which often showed intraspecific geographical differences not attributable to anthropogenic effects. Cadmium concentrations in Themisto species are high in comparison with those of other oceanic crustaceans and may represent significant sources of cadmium in the diets of particular seabrids.