special number 1. the biology of the antarctic krill euphausia superba: proceedings of the first...

LIPID CONTENT AND COMPOSITION OF ANTARCTIC KRILL, EUPHAUSIA SUPERBA DANAAuthor(s): Andrew ClarkeSource: Journal of Crustacean Biology, Vol. 4, Special Number 1. THE BIOLOGY OF THEANTARCTIC KRILL EUPHAUSIA SUPERBA: Proceedings of the First International Symposiumon Krill held at Wilmington, North Carolina, from 16-19 October 1982 (November 1984), pp.285-294Published by: The Crustacean SocietyStable URL: http://www.jstor.org/stable/27920104 .

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JOURNAL OF CRUSTACEAN BIOLOGY, 4 (SPEC. NO. 1): 285-294, 1984

LIPID CONTENT AND COMPOSITION OF ANTARCTIC KRILL, EUPHAUSIA SUPERBA DANA

Andrew Clarke

ABSTRACT

Available data on the lipid content and composition of the Antarctic krill Euphausia superba Dana are summarized. Female total lipid content increases during the summer as

the ovary matures, and there is also some evidence of an increase in the lipid content of males and immatures as winter approaches. The storage lipid is mainly triacylglycerol and there is less than 1% wax ester. Fatty acids are moderately unsaturated, though less so in the ovarian lipid, and the triacylglycerol contains up to 4% phytanic acid. These data suggest that krill feed on phytoplankton during the summer bloom, but that, unlike E. crystalloro

phias, E. superba does not rely on a lipid store to survive the winter.

Current knowledge of the lipid biochemistry of Euphausia superba is limited. All samples have been taken in summer, and in relatively few cases have these been sorted according to size, moult stage, sex, or sample depth, all of which are factors liable to influence the lipid composition of krill.

Even less is known of other Antarctic euphausiids, although recently there have been detailed studies of the biology and lipid biochemistry of three species of such crustaceans in the Arctic. This paper summarises existing data for E. superba, and contrasts these with information for other polar euphausiids. Consideration of krill physiology, life history, and the polar environment suggest several areas where further biochemical research is needed.

Available Data

Lipid content of Euphausia superba

Although there have been many analyses of lipids of krill, few have considered variation with sex, age, or water depth. For example, Ferguson and Raymont (1974) described an increase in lipid content with size in krill from the west

Atlantic sector of the Southern Ocean collected in December-February, but since the larger krill may have contained mature females with large ovaries this trend possibly reflects only the effect of sexual maturation, not size per se.

Data on the total lipid content of krill are given in Table 1, broken down according to sex and date. Two features are apparent. Firstly, mature female krill contain more lipid than mature males (except possibly late in the summer), and secondly, the lipid content of each sex varies with time. Thus, in both male and immature krill from South Georgia, samples in late summer were richer in lipid than those taken earlier (Clarke, 1980). When all the available data are plotted against time (Fig. 1) there is a distinct tendency for lipid content to increase towards the onset of winter, although with so few samples it is not possible to be definitive. Raymont et al. (1971) reported an increase in the lipid content of immature and adolescent krill (300-600 mg wet wt) from 12.96% dry wt (standard error = 0.88,

= 26) in December, to 27.06 ? 1.10% (N= 8) in January; these

are equivalent to 2.60 and 5.41% wet wt, respectively (Table 1). Ferguson and

Raymont (1974) also reported an increase in lipid from 16.1% dry wt in late December to 34.4% dry wt in February (3.22 and 6.88% wet wt, respectively), and an increase in mean lipid content from about 15% dry wt in December to about 20% in April was reported by Roschke and Shreiber (1977). In neither case,

285



286 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 4, SPEC. NO. 1, 1984

Table 1. Total lipid content of Euphausia superba. All data % fresh wt, mean ? standard error with number of individuals in parentheses.

* indicates an estimated value calculated from data provided as % dry wt, on the assumption of a water content of 80%.

Total lipid Remarks

Immatures and adolescents

15-18 Dec 2.61* (26)

21 Jan

23 Jan

4.09 ? 0.39(11)

5.41* (8)

19 1 2 11

Feb Mar Mar Mar

4.9 6.49 4.4 7.2

17 19 28

22

2.78 (2)

Mature males

3 Feb 1 Mar 2 Mar 11 Mar

Mature females

29 Jan 3 Feb 8 Feb 13 Feb 19 Feb 21 Feb

1 Mar 2 Mar

11 Mar

Pooled samples

28 Dec Jan Jan Jan Jan Feb Mar

2.41 ? 0.48 (8) 5.33 ? 1.04(12) 1.6 1.8

5.72 ? 0.57 (9) 5.23 ? 0.24 (8) 6.01 ? 0.46 (3) 5.63 ? 0.23 (6) 2.8 5.30 ? 0.33(13) 6.33 ? 0.49 (20) 4.2 4.9

3.22* (8) 3.82* (8) 6.22* (10) 5.52* (8) 5.21* 6.88* (22) 2.13*

12.96 ? 0.88% dry wt; data for 4 sampling dates combined; 300 600 mg wet wt; Antarctic Peninsula, 66?S, 69-70?W; Raymont et al, 1971.

South Georgia; Clarke, 1980 (where incorrectly reported as 21

Feb). 27.06 ? 1.10% dry wt, Antarctic Peninsula, 66?S, 69-70?W; Ray

mont et al, 1971. No position given; Kryuchkova and Makarov, 1969. South Georgia; Clarke, 1980. No position given; Kryuchkova and Makarov, 1969. No position given; Kryuchkova and Makarov, 1969.

South Georgia; Clarke, 1980. South Georgia; Clarke, 1980. No position given; Kryuchkova and Makarov, 1969. No position given; Kryuchkova and Makarov, 1969.

Bransfield Strait; Clarke, 1980. South Georgia; Clarke, 1980. South Georgia; Clarke, 1980. South Georgia; Clarke, 1980. No position given; Kryuchkova and Makarov, South Georgia; Clarke, 1980. South Georgia; Clarke, 1980. No position given; Kryuchkova and Makarov, No position given; Kryuchkova and Makarov,

1969.

1969. 1969.

62?S, 56?W; Bransfield Strait; Ferguson and Raymont, 1974.

61?S, 48?W; Scotia Sea; Ferguson and Raymont, 1974.

58?S, 40?W; Scotia Sea; Ferguson and Raymont, 1974.

54?S, 35?W; South Georgia; Ferguson and Raymont, 1974. Weddell Sea, Atlantic sector; Vinogradova, 1960.

54?S, 34?W; South Georgia; Ferguson and Raymont, 1974. Ross Sea, near Balleny Is.; Vinogradova, 1960.

Pooled samples taken on unspecific dates

5.17 66?S, 136?W in West Wind Drift; Hansen and Meiklen, 1970. 3.41 OffEnderby Land; Tsuyujki and Itoh, 1976.

5.48* Ross Sea; Sidhu et al, 1970. 3.74* Van der Veen et al, 1971. 3.88* Sample from stomach of fin whale; Nonaka and Koizumi, 1964.

however, were the sexes analysed separately, and so it is not clear whether males and immatures are storing lipid as well as females. Kryuchkova and Makarov

(1969), however, found an increase in the lipid content of both females and immatures in February and March, and the lipid content of late summer im

matures was very high indeed. If male and immature krill (neither of which require large lipid stores for

reproduction) are synthesising an overwintering lipid reserve, two questions im

mediately suggest themselves: (1) Why is this synthesis apparent in late summer,



CLARKE: LIPIDS OF EUPHAUSIA SUPERBA 287

Dec Jan Feb Mar

Fig. 1. Total lipid content (% fresh weight) of male (O) and immature (?) Euphausia superba in summer. Data are from Table 1, and plotted as mean ? standard error where data available.

rather than at the period of peak phytoplankton abundance, and (2) What is the nature of the storage lipid?

To answer the first question requires better knowledge than we have at present of the relationship between krill feeding and lipid storage; the second question is discussed in the ne^t section.

Female krill cle?rly store large quantities of lipid for reproduction. Close to

spawning, the mature ovary swells the thorax markedly and can contain 60% of the total lipid in the female krill (Clarke, 1980). Data from gravid and spent females in the same net haul (note that this does not necessarily mean that they came from the same swarm) suggest that at spawning a female loses about 54% of her total lipid (Table 2). Although these observations might suggest that the whole ovary is spawned at once, this may be the result of shock following capture in the net, since recent evidence indicates that in the wild spawning proceeds gradually over a number of days or weeks (Denys and McWhinnie, 1982).

Two determinations of the lipid content of a krill egg gave a mean of 9.435 Mg; this allows an estimation of krill fecundity from lipid composition (Table 3). These estimates are within the range of values collated by Everson (1977), but are likely to be underestimates (Denys and McWhinnie, 1982). George (pp. 252

262, this number) found less lipid in krill eggs from females taken off Elephant Island.

The total lipid contents reported for E. superba are not especially high for

zooplankton. Several other Antarctic euphausiids are richer in lipid (for example, E. frigida, 19.4% wet wt; Clarke, 1983). There is no indication of variation in

lipid content with area, although data are very scanty. The major need is for a better understanding of seasonal variations in total lipid content, particularly in the period leading up to winter. This is important not only in terms of an un




Table 2. Loss of lipid at spawning in female Euphausia superba at South Georgia, 1978; all data are mean ? standard error (from Clarke, 1980).

Haul RMT 176, 8 Feb 1978, 0130 h, surface, 56?35'S, 36?34'W.

Mean fresh weight mature females: 1.64 ? 0.11 g ( =

8)

Total lipid content of gravid females: 6.01 ? 0.46 % fresh wt (N =

5) Total lipid content of spent females: 2.79 ? 0.36 % fresh wt (N

= 3)

This indicates a loss of 54% of the total lipid in a female krill at spawning.

derstanding of the energy budget of E. superba (Clarke and Morris, 1984), but also the nutritive value of krill to its predators.

Lipid Composition of Euphausia superba

The major lipid classes of Euphausia superba are phospholipid, free sterol, and

triacylglycerol (Bottino, 1975; Clarke, 1980). Some samples, but not all, contain up to 10% free fatty acid, though this may be due in part to autolysis.

The wax ester content of E. superba is <1% (Clarke, 1980). It is currently believed that wax esters are synthesised in preference to triacylglycerol when

organisms must make maximal use of a sporadic, seasonal, or unpredictable food supply (see Sargent, 1976), the classic example being copepods, especially in polar regions. That E. superba contains only traces of wax ester would suggest that it is not dependent on a single food source of limited availability (for example, diatoms), but is omnivorous and/or can feed year-round. This in turn would suggest that there is no need for an overwintering store of lipid, which is contrary to the limited data for male and immature krill in late summer (Fig. 1; Table 1). An increasing amount of both anecdotal and observational data suggest that E.

superba is indeed an omnivore, with the ability to feed on a wide range of particle sizes (Clarke and Morris, 1984; Morris, pp. 185-197, this number; Boyd et al. pp. 123-141, this number). The need for winter samples of krill is obvious.

The fatty acids of E. superba are moderately unsaturated; in males, phospholipid contains 24% 20:5 3 and 25% 22:6a>3, triacylglycerol 11% 20:5 3 and 3% 22:6 3. Ovarian lipids are less unsaturated, and ovarian triacylglycerol contains

Table 3. Calculation of the fecundity of Euphausia superba from lipid data; South Georgia, 1978

(from Clarke, 1980).

Assume that a mature female krill contains 6.3% lipid (maximum recorded, 1 Mar 1978). Assume that 54% of this is lost at spawning (Table 2). A single krill egg contains 9.435 g lipid.*

Gravid female fresh weight Lipid lost at spawning g mg Estimated number of eggs

2 68.4 7,200 3 102.5 10,000 4 136.7 14,500

* Mean of two determinations from eggs obtained from gravid female krill allowed to spawn in the laboratory. Eggs were sorted under a stereomicroscope and only live (clear) eggs used for analysis. 17 Feb 78: 167 eggs contained 1.6 mg lipid (9.58 % per egg). 3 Mar 78: 1,184 eggs contained 11.0 mg lipid (9.29 % per egg).



Table 4.

CLARKE: LIPIDS OF EUPHAUSIA SUPERBA

Carotenoid pigments of Euphausia superba (Czeczuga and Kfyszejko, 1977).

289

Carotenoid pigment content

% g-1 fresh wt % total pigment

Hydroxy-^-carotene 3.41 21.7

Dihydroxy-f-carotene 0.24 1.5

Cryptoxanthin 4.37 27.8

Flavoxanthin 1.71 10.9 Zeaxanthin 2.04 13.0 Astaxanthin 1.16 7.4

Astaxanthin ester 2.78 17.7

Total 15.71

only 11.7% polyunsaturated fatty acids (Clarke, 1980). The small amounts of

polyunsaturated fatty acids in ovarian (and hence egg) lipids, compared with other

crustaceans, are probably related to the relatively short period the larvae must survive before they can feed for themselves (Clarke and Morris, 1984).

Fatty acid composition, particularly that of triacyglycerol, is influenced greatly by dietary input, and so will vary from sample to sample. One unusual feature, however, is the high content of phytanic acid (3,7,11,15-tetramethylhexadecanoic acid). The presence of this isoprenoid acid in Antarctic krill was first demonstrated

by precision open-tubular column gas chromatography, mass spectrometry, and infrared spectrophotometry, following a complex isolation procedure (Ackman and Hansen, 1967; Hansen and Meiklen, 1970). Phytanic acid constituted 1.4% of total fatty acids in krill from the West Wind Drift (136?W, 66?S) and two other

isoprenoid fatty acids were also detected: pristanic acid (2,6,10,14-tetramethyl pentadecanoic acid, 0.04%) and 4,8,12-trimethyltridecanoic acid (0.05%). Small amounts of these acids have also been found in Meganyctiphanes norvegica and

Thysanoessa inermis (Ackman et a , 1970). The derivation of pristane and phy tanic acid from the phytol moiety of chlorophyll (Avigan and Blumer, 1968), and the unusually high levels of phytanic acid in krill triacylglycerol together with the

typical algal fatty acids 16:4 3 (1.16%) and 18:4 3 (1.47%) indicate that in sum mer krill are feeding intensively on diatoms. A detailed analysis of the total fatty acids (lipid classes were not separated before analysis) of E. superba has also

recently been reported by Golovnya et al. (1981), who used capillary gas chro

matography, together with hydrog?nation and mass spectrometry to confirm iden tification. Eighty-three fatty acids were found, including 2.8% phytanic acid and traces of other isoprenoids, 0.3% or less of 11 monomethyl branched acids, 0.5% 16:4 1, 1.6% 18:4a>3, 16.0% 20:5<o3, and 8.4% 22:6a>3. The isomer ratio 18:1 7/18:1a>9 was 0.48, lower than that reported by Clarke (1980) for either

phospholipid or triacylglycerol analysed separately. Generally similar fatty acid compositions have been reported by Pierce et al.

(1969), Sidhu et al. (1970), Bottino (1974, 1975), and van der Veen et al (1971). Tsuyuki and Itoh (1976) found only 12.6% 20:5 3 and 0.7% 22:6 3 in total fatty acids (although they did report 11.3% of the unusual fatty acid 22:3) and almost all of these polyunsaturated acids were in the free fatty acids. Krill Upases are

very active, and, although these krill were frozen, the very high free fatty acid content (27% total lipids) indicates that extensive autolysis had taken place. Rel

atively high levels of polyunsaturated fatty acids were reported by Nonaka and Koizumi (1964) in krill samples from the stomach of a fin whale, but the complex fractionation procedure employed makes comparison with more recent studies



290

Table 5.

JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 4, SPEC. NO. 1, 1984

Lipid content and composition of Southern Ocean euphausiids (from Clarke, 1983).

Total lipid

Species % Fresh wt

Lipid class composi tion

% total lipid

Tr? Phos- acyl - pho- glyc- Wax

% Dry wt lipid eroi esters

E. superba E. superba gravid E. superba spent E. crystallorophias

E. crystallorophias E. crystallorophias E. frigida

E. triacantha

Thysanoessa sp.

2.41-5.33 5.23-6.33

2.79 ? 0.36

2.79

19.38

9.40-35.5 - -

4.03

5.33

41 22 < 1 = 20; Clarke, 1980. 39 29 < 1 = 59; Clarke, 1980. - - - N= 5; Clarke, 1980. ? ? ? =

6, single pooled sample; Clarke, unpublished observation.

Seasonal study; Littlepage, 1964. 53 - 46 Pooled sample; Bottino, 1975.

= 3; single pooled sample;

Clarke, unpublished observation.

N= 10; single pooled sample; Clarke, unpublished observation.

N= 3; single pooled sample; Clarke, unpublished observation.

difficult. These and other early studies (e.g., Saiki et ai, 1959) have been collated

by Grantham (1977).

Carotenoid Pigments

When removed from a net sample, the colour of krill can range from almost clear to deep red. These changes are, however, due mostly to variations in chro

matophore extension rather than total pigment content (Clarke, 1980). The relationship between total pigment content (assayed as astaxanthin) and

fresh weight (W, in g) may be expressed by the power relation: total pigment (Mg)

= 20.09 W? 768 ? 0 ?96. This relationship is based on 90 individual krill taken from around South Georgia. The weight exponent is not significantly different from 0.67 (t

= 1.03, > 0.05) suggesting that pigment content increases ap

proximately with surface area (Clarke, 1980). The individual carotenoid pigments have been identified and qualified by col

umn and thin-layer chromatography by Czeczuga and Kfyszejko (1977). In ad dition to the astaxanthin and astaxanthin ester to be expected, several unusual carotenoids were reported, including flavoxanthin (Table 4).

Discussion

Comparison with Other Antarctic Euphausiids

The only other Antarctic euphausiid for which good data are available is E.

crystallorophias. A seasonal study of the total lipid content showed that during winter under the fast ice, the lipid content steadily decreased (Fig. 2). This must

represent the effect of metabolic demands on the lipid reserves, since, although egg maturation is proceeding in the ovary, merely transferring lipid from the hepatopancreas to the ovary will not affect total lipid content. Eggs are released to the plankton in summer, and when phytoplankton food is once more available

lipid reserves are rapidly resynthesised (Fig. 2). This study shows clearly that E.




I 10

Fig. 2. Seasonal variation in total lipid content (% fresh weight) of Euphausia crystallorophias at McMurdo Sound, 1961-62. Data plotted are values for pooled samples, sexes mixed, from double vertical hauls 0-290-0 m, from Stanford collecting site 6 IB, 25 km SE of McMurdo Station (77?50'S, 166?40 ) in the southwestern Ross Sea. The bar shows the period during which euphausiid eggs are

present in the plankton (redrawn from Littlepage, 1964). Data for chlorophyll a are for Stanford

collecting site 62B, 20 m depth, 1962-63. Redrawn from fig. 5 in Bunt, 1964.

crystallorophias stores lipid during summer for use over winter when food is unavailable, and, as would be expected, much of this lipid is wax ester (Bottino, 1975). There are very few data for other Southern Ocean euphausiids (Table 5). The

smaller species are generally richer in lipid, and at least two contain substantial amounts of wax ester.

Arctic Euphausiids

The most detailed studies of Arctic euphausiids have concentrated on three

species which coexist in Balsfjorden, northern Norway (69?N), Meganyctiphanes norvegica, Thysanoessa inermis, and T. rasch?i. Meganyctiphanes norvegica is not a stable member of the community, however, since it does not spawn in the fjord. In all three species spawning takes place in spring and early summer, the exact

timing depending on the latitude, and lipid accumulates during summer. The exact pattern, however, varies with species and also with area.

Meganyctiphanes norvegica is carnivorous, feeding extensively on wax-rich co

pepods, but storing only triacylglycerol. Lipid accumulates over winter, indicating feeding, although little growth occurs then. Thysanoessa inermis is an omnivore and stores both wax ester and triacylglycerol. There is a striking parallel between

primary productivity and lipid content, indicating that T. inermis relies to a large extent on phytoplankton food. Although the fatty acids contain no phytanic acid,




the wax alcohols contain 10% phytol. Thysanoessa rasch?i also stores both wax ester and triacylglycerol, and in winter the wax alcohols are almost exclusively (90%) phytol. This suggests that T. rasch?i is highly dependent on phytoplankton food, and in winter possibly also feeds on detritus (Falk-Petersen, 1981; Falk Petersen et a , 1981 ; Sargent and Falk-Petersen, 1981 ; Falk-Petersen et al, 1982).

In all three species lipid contents are variable, but can rise as high as 14% fresh

weight. Specimens from other areas are sometimes comparable in lipid content

(T. inermis, Frobisher Bay, northern Canada, 13.7%; Percy and Fife, 1981), and sometimes not (T. rasch?i, Bering Sea, 1.3%; Ikeda, 1972).

Conclusions

Available data for polar euphausiids indicate that there is an intimate but

complex interrelationship between feeding ecology and lipid biochemistry. In

particular, the degree of dependence on phytoplankton food may dictate whether

lipid reserves for winter are large or small, and whether they are primarily tri

acylglycerol or wax ester (Sargent, 1976; Clarke, 1983). These generalisations suggest that E. superba is probably an omnivore, and able to feed year-round. This in turn would suggest that there is no need for an overwintering lipid store, despite the indications in Fig. 1, and that lipid composition, in particular tria

cylyglycerol fatty acid composition, will vary from sample to sample depending on recent feeding history.

Clearly there is a need for a full seasonal study of the lipid biochemistry of E.

superba, taking into account sampling area, depth, moult stage, sex, and age, and

particularly in relation to feeding ecology.

Acknowledgements

I would like to thank Dr. J. R. Sargent for many useful discussions of lipid biochemistry of krill, Dr. I. Everson for constructive criticism of an early draft, and Christine Phillips for help with Russian and Japanese publications.

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Accepted: 18 July 1983.

Address: British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 OET, United Kingdom.



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