Comparative lipid dynamics of euphausiids from the Antarctic and Northeast Pacific Oceans

To better understand the feeding and reproductive ecology of euphausiids (krill) in different ocean environments, lipid classes and individual lipid components of four different species of euphausiids from Northeast Pacific (temperate species) and Southern Ocean (Antarctic species) were analyzed in animals from multiple life stages and seasons. The dominant krill species in the Northeast Pacific Euphausia pacifica and Thysanoessa spinifera, were compared to the two major Antarctic species, Euphausia superba and E. crystallorophias. Analysis comprised total lipid and lipid classes together with individual fatty acid and sterol composition in adults, juveniles, and larvae. Antarctic krill had much higher lipid content than their temperate relatives (10–50 and 5–20% of dry mass for Antarctic and temperate species, respectively) with significant seasonal variations observed. Phospholipids were the dominant lipid class in both temperate krill species, while neutral storage lipids (wax esters and triacylglycerols for E. crystallorophias and E. superba, respectively) were the major lipid class in Antarctic krill and accounted for up to 40% of the total lipid content. Important fatty acids, specifically 16:0, 18:1ω9, 20:5ω3, and 22:6ω3, were detected in all four krill species, with minor differences between species and seasons. Detailed lipid profiles suggest that krill alter their lipid composition with life stage and season. In particular, larval Antarctic krill appear to utilize alternate food resources (i.e., sea-ice associated organisms) during austral winter in contrast to juveniles and adults (i.e., seston and copepods). Lipid dynamics in krill among krill in both systems appear closely linked to their life cycle and environmental conditions including food availability, and can provide a more complete comparative ecology of euphausiids in these environmentally distinct systems.     

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     

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.     

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.     

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     

Fatty acid signature analysis documents the diet of five myctophid fish from the Southern Ocean

Fatty acid (FA) and fatty alcohol (FAlc) compositions of both total lipid and neutral lipid fractions were studied for five myctophid species sampled in Kerguelen waters. Both qualitative and quantitative FA signature analyses were then performed to investigate their diet over longer time scales than the conventional stomach content analysis. Regarding their lipid class, FA and FAlc compositions, the five species could be discriminated into two groups: wax-ester-rich species (Electrona antarctica, Krefftichthys anderssoni) characterised by large amounts of monounsaturated FAs (>73% of total FAs) and triacylglycerol-rich species (Electrona carlsbergi, Gymnoscopelus nicholsi, Protomyctophum bolini) with major amounts of saturated and monounsaturated FAs (>29 and >46% of total FAs, respectively). Qualitative and quantitative FA analyses showed that K. anderssoni mainly preyed upon copepods, E. antarctica upon copepods and more euphausiids and P. bolini and E. carlsbergi mainly upon euphausiids with some copepods, while G. nicholsi had a more diverse diet. This study shows the usefulness of quantitative statistical analysis to determine the diet of Antarctic and sub-Antarctic predators and stresses the need of increasing the lipid and FA analyses of more zooplanktonic and micro-nektonic marine species.     

Ultrastructure of the integument of a pelagic Crustacean: moult cycle related studies on the Antarctic krill,Euphausia superba

The ultrastructure of euphausiid integument was examined in relation to the moult cycle and supplemented by investigations of chitinase activity in the integument and content of N-acetyl--D-glucosamine in the hemolymph. The Antarctic krill, Euphausia superba was collected in 1983 in Admiralty Bay, King George Island, Antarctica. Some specimens of the Northern krill, Meganyctiphanes norvegica, from the Danish Kattegat served for comparison. As a major aim of the study, the moult staging system developed for living tissue could be verified by ultrastructural findings. Under experimental high production conditions of the Antarctic summer, no period of rest or intermoult between post- and premoult was observed in subadult E. superba. Neither was a resting phase seen at the cellular level, the epidermis remained active. The epidermal gland cells did not show any cyclical changes, and the organelles of protein synthesis were generally well developed in all moult stages. In order to follow the physiological course of events, structural and biochemical methods were combined and showed as a result that the last moult stage before ecdysis is characterized by massive cuticular resorption. The epicuticle remained ultrastructurally unchanged before and after ecdysis, even though its permeability should alter at ecdysis. The existence of muscle insertions which connect the old and the new cuticle across the exuvial space suggests an answer to the question why E. superba is hardly impaired in swimming almost up to the time of ecdysis.Dedicated to Professor Dr. H. Leonhardt on the occasion of his 70th birthday     

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.     

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.     

Metabolic activity and elemental composition of krill and other zooplankton from Prydz Bay,Antarctica, during early summer (November–December)

Oxygen uptake and ammonia excretion rates, and body carbon and nitrogen contents were measured in krill (Euphausia superba) and eight other zooplankton species collected during November–December 1982 in the Prydz Bay, Antarctica. From these data, metabolic O:N ratios (by atoms), body C:N ratios (by weight) and daily metabolic losses of body carbon and nitrogen were calculated as a basis from which to evaluate seasonal differences in metabolism and nutritional condition. Comparison of the present data with mid-summer (January) data revealed that early-summer E. superba were characterized by higher metabolic O:N ratios (58.7 to 103, compared with 15.9 to 17.5 for mid-summer individuals). Higher O:N ratios of early-summer E. superba resulted largely from reduced ammonia excretion rates and, to a lesser degree, from slightly increased oxygen uptake rates. Body C:N ratios of E. superba were low in early-summer (3.8 to 4.2) compared with mid-summer krill (4.1 to 4.7) due to lowered body-carbon contents in the former (42.6 to 43.6% compared with 43.2 to 47.5% dry weight of midsummer individuals); gravid females formed an exception, since no seasonal differences in body elemental composition were detected for these. No significant changes in water content (75.3 to 81.4% wet wt) and nitrogen content (9.9 to 11.1% dry wt) in E. superba were evident between the two seasons. Seasonal differences in metabolic rates and elemental composition were less pronounced in a salp (Salpa thompsoni), but a higher metabolic O:N ratio occurred in early-summer individuals. Interspecific comparison of the seven remaining zooplankton species studied with twelve species from mid-summer zooplankton investigated in an earlier study indicated that higher metabolic O:N ratios in early-summer are characteristic not only of herbivore/filter-feeders, but also of some carnivores/omnivores. No relationship between metabolic O:N ratios and body C:N ratios was apparent either intraspecifically or interspecifically, within or between early-summer and mid-summer seasons.     

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.     

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.     

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     

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     

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.     

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     

Ammonium cycling by Antarctic zooplankton in winter

Elemental composition and excretion rates of ammonium-nitrogen of zooplankton, ranging over more than five orders of magnitude in body size, were measured in mid-winter in coastal waters west of the Antarctic Peninsula. Excretion rates were constant for the initial 12 h of incubation in the four species tested, and experimental stocking densities of up to 126 mg dry wt l^-1 did not cause variability in the rate of ammonium production. Weight-specific excretion rates of freshly caught Euchaeta antarctica, Conchoecia sp., Thysanoessa macrura, Euphausia superba, and early stage copepodites of Metridia gerlachei were not significantly different from those reported in summer. However, adult copepods of M. gerlachei and Calanoides acutus appear to have reduced their nitrogen metabolism during winter. Turnover rates of body nitrogen increased with diminishing size, ranging from <0.5% body N d^-1 for large E. superba to >7% body N d^-1 for CII and CIII copepodites of M. gerlachei. Only the nitrogen turnover rates of C. acutus were sufficiently low as to suggest that it could survive the entire austral winter without feeding. Phytoplankton and bacterioplankton were virtually absent in both the water column and the sea-ice. We conclude that carnivory is the dominant trophic mode of the pelagic zooplankton community in Antarctica during winter. Production of ammonium-nitrogen by the zooplankton community probably accounts for M10% of the total ammonium regenerated prior to the annual spring bloom.     

Omnivorous feeding behavior of the Antarctic krill Euphausia superba

Feeding experiments were conducted at Palmer Station from December 1985 to February 1986 to examine the potential role of copepod prey as an alternative food source for Euphausia superba. Copepod concentration, copepod size, phytoplankton concentration, the duration of krill starvation and the volume of experimental vessels were altered to determine effects on ingestion and clearance rates. Krill allowed to feed on phytoplankton and copepods in 50-litre tubs showed greatly increased feeding rates relative to animals feeding in the much smaller volumes of water traditionally used for krill-feeding studies. Clearance rates on copepods remained constant over the range of concentrations offered, but clearance rates on phytoplankton increased linearly with phytoplankton concentration. Feeding rates increased when larger copepods were offered and when krill were starved for two weeks prior to experiments. Clearance rates of krill feeding on copepods were higher than, but not correlated with, their clearance rates on phytoplankton in the same vessel. E. superba may have a distinct mechanism for capturing copepods, perhaps through mechanoreception. Although our observed clearance rate of 1055 ml krill^-1 h^-1 indicates that krill can feed very efficiently on copepod prey, such feeding would meet less than 10% of their minimum metabolic requirements at the typical copepod concentrations reported for Antarctic waters. However, substantial energy could be gained if krill fed on the patches of high copepod concentrations occasionally reported during the austral summer, or if krill and copepods were concentrated beneath the sea ice during the winter or spring months. Our results, indicating efficient feeding on zooplankton and higher clearance rates on phytoplankton than previously believed, represent a step towards balancing the energy budget of E. superba in Antarctic waters.     

Length-weight relationships and coefficient of condition of Euphausia superba and Thysanoessa macrura (Crustacea: Euphausiacea) in southwest Indian Ocean during summer

Samples of antarctic euphausiids, Euphausia superba and Thysanoessa macrura were obtained during the MD 25 FIBEX expedition of the R. V. Marion Dufresne, in February 1981, to the southwest Indian Ocean. Individual and mean coefficients of condition (K _m) were calculated from variations in weight as a function of total length and of carapace length. In E. superba, no significant differences were found as a function of sex or development stage in either total length and weight or carapace length and weight. In T. macrura, a significant allometric difference emerged in the wet weight of juveniles, males and females as a function of total length, and in wet weight as a function of carapace length between adults and subadults. In both E. superba and T. macrura, wet weight as a function of total length differed significantly among stations, and also between species, with a greater weight increase for T. macrura in summer. The coefficients of condition calculated for all wet weight-total length relationships showed that the morphologically different Group II males were heavier than Group I males and mature females. K _m in T. macrura was higher for females than for juveniles or males, indicating a greater weight gain by the females. These differences probably reflect real differences in physiology and may affect the distribution of these two species.