Ecological investigations on the zooplankton community of Balsfjorden, northern Norway: Seasonal changes in body weight and the main biochemical composition of thysanoessa inermis (krøyer), T. Raschii (M. Sars), and Meganyctiphanes norvegica (M. Sars) in relation to environmental factors

J. exp. nrar. Biol. Ecol., 1981, Vol. 49, pp. 1033120 0 Elsevier/North-Holland Biomedical Press

ECOLOGICAL INVESTIGATIONS ON THE ZOOPLANKTON COMMUNITY OF BALSFJORDEN, NORTHERN NORWAY: SEASONAL CHANGES IN BODY WEIGHT AND THE MAIN BIOCHEMICAL COMPOSITION

OF TH YSANOESSA

T. RASCHZZ (M. Sars), AND MEGANYCTZPHANES

ZNERMZS (Krsyer),

NORVEGZCA

(M. Sam)

IN RELATION TO ENVIRONMENTAL FACTORS

STIG

FALK-PETERSEN

Aquatic Biology Group, Itlstitute qf’Biology and Geology, University qf Tromso, P.O. Box 790, 9001 Tromso, Nowa!> Abstract: An eco-biochemical study of the euphausiids Thysanoessa inermis (Kroyer). T. raschii (M. Sars), and Meganyctiphanes norvegica (M. Sars) has been carried out in Balsfjorden. northern Norway. (70 “N). The seasonal variation in wet and dry weights, and protein, lipid, and ash content of 0-, I- and IIgroups have been related to their population dynamics and to environmental data. The weight increases and changes in biochemical content were closely related to the primary production cycle. Ogroup Thysanoessa showed an increase in weight from July to September, while there was “stagnation” during the winter. In I-group of the two Thvsanoessa species a great increase in weight could be seen from March-April to August-September; wet and dry weights, and protein and lipid contents inDuring winter the weight decrease in I-group creased by >350, 600. 500, and 1200”,,, respectively. ThJsanoessa could partly be explained by a decrease in the mean carapace length of the population. The proportion of protein and ash was higher and lipid lower in the O-group than in I- and II-groups for the three investigated species. The decrease in the relative amount of lipid in the O-group Thysanoessa during winter can be related to both low phytoplankton production and decreasing food quality. There was a decrease in lipid for I-group T. inermis and Mcgan_vctiphanes norvegica during the winter and this can be associated with the use of energy for over-wintering and growth of gonads. The difference in the protein/lipid content between the three species indicate different metabolic responses towards overwintering. The uses of biochemical variation in examination of ecological niches are discussed and it is suggested that the high lipid level (487;) in I-group Thj~sanoessa inermis indicates that this species is a more “obligate” herbivore than I-group T. raschii and Megan~wiphanes norvegica with lower lipid levels (= 37”“). The biochemical composition for the three species from different geographical areas have been compared. The lipid contents were considerably higher in euphausiids from the subarctic Balsfjorden (70”N) than those levels published for temperate-boreal waters (5O60”N). This supports the supposition that lipid is especially important in the ecology of zooplankton from higher latitudes, It is concluded that differences in lipid levels between zooplankton from different latitudes reflect differences in light climate and its influence on primary production.

INTRODUCTION

The biochemical

composition

of planktonic

organisms

has been studied

since the

pioneering work of Brandt (1898) and Brandt & Rabben (1922). In boreal waters the influence of the environment and season on the biochemical composition of species 103

104

STIG FALK-PETERSEN

has been investigated around the British Isles (Raymont et al., 1966, 1969a, b, 1971) as well as in fjords in western Norway (Bamstedt, 1975, 1976, 1978). There are, however, few studieswhich combine information from environmental factors, population dynamics, and the biochemical variations of the animal’s body to further our understanding of the animal’s biology. It has also been shown that a knowledge of the changes in basic biochemical composition is necessary to understand overwintering behaviour (Iles, 1974). Growth and metabolism in zooplankton from Arctic and subarctic latitudes must, of necessity, be well adapted to conditions found in these regions. Zooplankton need to grow and synthesize enough energy-rich reserves during the short primary production season in order to survive the long winter and to breed the following spring. For filter-feeding zooplankton, which are mainly dependent upon phytoplankton or micro-zooplankton associated with phytoplankton (see Conover, 1964), it is thought that lipids function as the chief energy reserve (Lee, 1974). It has been suggested that marine zooplankton from high latitudes have a higher lipid content than zooplankton from lower latitudes (Sheard, 1953; Littlepage, 1964) and the importance of lipid in marine zooplankton from high latitudes has been stressed by several authors (Raymont et al., 1969a; Lee, 1975; Benson & Lee, 1975). Lee (1975) considered that storage of lipid, especially wax esters, is an important aspect of the ecology of Arctic plankton. In recent years interest has been shown in the importance of krill, especially in Antarctic waters where commercial fisheries for krill have already started (see Eddie, 1977; Backus, 1978). Krill from northern latitudes has also been found in large quantities in sound-scattering layers from fjords in North Norway (Hopkins et al., 1978), and it may become a target for a future fishery. The economic yield and management of a krill fishery will depend, amongst other factors, on knowledge of the population structure and the biochemical composition of the animals (FalkPetersen & Hopkins, 1979). Ecological studies on the zooplankton community of Balsfjorden have been carried out since 1976. The fjord is well suited for ecological studies, and presents itself as a semi-enclosed ecosystem with an “out of phase” light-temperature regime. The maximum primary production is in spring when the water masses are still cold and homogeneous. In addition, variable light regimes are found, ranging from the midnight sun during summer to full darkness during the polar winter (Eilertsen et al., in press). Population dynamics of the three euphausiids Thysanoessa inermis, T. raschii and Meganycriphanes norvegica in Balsfjorden have previously been examined (FalkPetersen & Hopkins, in press) and the present paper presents data from an ecobiochemical study carried out simultaneously on the same population. The wet and dry weights, and protein, lipid, and ash contents of the euphausiids ThySanoessa inermis (Kroyer), T. raschii (M. Sars), and Meganyctiphanes norvegica (M. Sars) have been investigated in Balsfjord between May 1976 and July 1977.

ECO-BIOCHEMISTRYOFEUPHAUSIIDS

105

Carbohydrates were not determined because they account for only a minor part of the body content of zooplankton (Raymont et al., 1969a; Bamstedt, 1978). Seasonal changes in the results are presented and discussed in relation to the animals’ life cycles and environmental variables.

MATERIALANDMETHODS

The sampling station was located near Svartnes, Balsfjorden (69”2l’N : 19”06’E) where the depth is 180-190 m. Further details of the area are given in Eilertsen et al. (in press). Seasonal changes in phytoplankton cell-counts, salinity, and temperature for the period under investigation are given in Falk-Petersen & Hopkins (in press). Incident and subsurface irradiance, nutrient analyses of the sea water, primary production, and further details of the phytoplankton cell-counts are given in Eilertsen (1979). Details of the zooplankton sampling are given in Falk-Petersen & Hopkins (in press). Live animals for weight measurements and biochemical analyses were individually picked out from a container tilled with sea water, carefully packed in single layers in small plastic bags and frozen in liquid nitrogen (- 196 “C). The samples were stored at - 20 “C until analysed. Wet-weight measurements were standardized following suggestions made by Winberg (1971). The frozen samples were melted in sea water, quickly rinsed in distilled water, and excess water soaked-up in filter-paper. The individual animals were then placed in tared aluminium containers for weighing. The animals were dried in a desiccator in vacua with self-indicating silica gel for = 14 days (Lovegrove, 1966) and re-weighed before biochemical analysis. Individuals used for ash weights were burned in a muffle furnace at 540 “C for 10 h (see Grove et al., 1961) and cooled to room temperature before weighing. Weighings were carried out on the following balances according to the size of the samples: Sauter Feinwage 404/13 (accuracy + 100 pg), Sartorius 2405 (accuracy + 1 pg) or a Sartorius electronic 4413 (accuracy * 2 pg). Biochemical analyses were carried out on individual animals if their dry weight was > 5 mg; smaller animals were pooled for analysis. Total protein was estimated TABI F I

Thysanoessa inermis, T. radii and Megangctiphws norvrgica: regression equations for total lipid (pg) against extinction (at 520 nm) are given by an equation of the type Y = hX + a; n, number of samples; h, regression coefficients, d.f.. degrees of freedom; r, correlation coefficient. Species

n

Range Wg/ml)

h

(I

d.f.

I

M. norvegica T. radii T. krmis

9 9 6

O-752.71 O-701.40 o-417.65

706.77 703.66 467.80

24.59 22.04 33.43

16 I5 12

0.993 0.993 0.993

106

STIGFALK-PETERSEN

by the biuret method of Gornall ef aE. (1949). TotaI lipid was extracted using the method of Folch et al. (1957) and analysed by the calorimetric SulphophosphovaniIin method given by Barnes & Blackstock (1973) but following the modifications of Bgmstedt (1975, 1976). Regression equations for the three species for total lipid and extinction are given in Table I. The regression equation for total protein (pg) and extinction (550 nm) is given by: Y = 17945X - 720, (v = 0.999, P < 0.001, d.f. = 15). Euphausiid identifications were based upon Einarsson (1945) and the animals were considered to change year-classes on 3 I March each year. The various generations were separated as given in Falk-Petersen & Hopkins (in press).

RESULTS

The monthly results of the analyses of generations I-III (GI-GIII) of ThJIsanoessa inermis, 7’. raschii, and Megunyctiphanes norvegica are presented in Tables II, III and IV. Sampling dates are given in Falk-Petersen, 1979. Seasonal variations in these results are shown in Figs. 1, 2, and 3 where the terms 0-, I- and II-groups are used to better relate changes in the measured quantities to the animals’ life cycles. Seasonal variations in the percentages of protein, lipid, and ash of body dry weight are given in Fig. 4.

In the O-group there was a general increase in the mass units (wet and dry weights, and protein and lipid contents) from July to September. The relative amount of protein was high until the middle of October (43-55%) whilst lipid accounted for only x 307;. The results from the two sampling dates in October are shown separately to demonstrate the marked change in the protein/lipid ratio; protein decreased from 53 to 40% of body dry weight whilst lipid increased from 32 to 43%. During the winter, from September to March, wet and dry weights, and protein content remained fairly stable, while there was a marked decline in the lipid content (1.820.69 mg) between January and February. The relative amount of protein decreased from the beginning of October to a minimum (x 35y0) in January before a marked increase in February, whilst lipid decreased from the end of October and reached a minimum (% 22%) in February. The relative amount of ash decreased from a maximum (29%) in February to a minimum (a 15~~) in November-December before there was a slight increase between February and April (x 18%). In the I-group there was a rapid increase in the mass units between April and September, wet weight increased by 35404 (25.08-l 13.80 mg), dry weight by 667’?,, (4.91-37.64 mg), protein by 470% (2.12-12.08 mg) lipid by 11650/, (1.42-17.96 mg), and ash by 3.57% (0.74-3.38 mg). A possible less intense growth period can be seen during mid-summer. Lipid became the dominant biochemical component in

ECU-BIUCHEMKSTKYUFEUPHAUSIiDS

107

108

STIG FALK-PETERSEN

the autumn accounting for = 50% of dry body weight. During the first month of the rapid weight increase I-group T. intwnis (and T. raschii) developed secondary sexual characters and some of the individuals became sexually mature (Falk-Petersen & Hopkins, in press). There were decreases in all quantities in the I-group with the

f GO36_

-ov--o--a--

Wet weight Dry weight Protein Lipid

-.-

Ash

- 120 -100

h g ”

-80

5 W

32 -

G

III

28

-60

tl 3

-40

t;

t

24 -

-

2rY

-0

3

20

J'A'S'O'N'D'J'F'M'd'M'J'

Fig. I. T/~~.~noc~u inrrrnis: seasonal variations in the mean wet, dry. protein, lipid. and ash weights and 95’;; confidence intervals for 0-, I-. and II-groups; confidence intervals for protein. lipid, and ash for O-group are shown in Table II: the axes are broken between GIII and GII; kkfjorden. North Norway.

onset of winter (about October). Wet weight and protein content appeared to have stabilized after December-January, whilst dry weight and lipid content continued to decrease until April, except for a possible slight increase in February. Dry weight was almost halved during this period (October-February). The marked decrease in dry weight and Iipid from February to April occurred at the same time as transference of spermatophores and spawning. Lipid accounted for QS5004 of dry body weight from August until January before a continuous decrease occurred from January until March (52-36”/,). After a decrease in the relative amount of protein (53 to =30?$ in spring, protein was stable (=30”/,) to January, before increasing to Z 35%.

ECO-BIOCHEMISTRY

109

OF EUPHAUSIIDS

In the II-group the weight increase started in April, and can be followed to JuneJuly when the majority of the animals died (Falk-Petersen & Hopkins, ,in press). There was an increase in the relative amount of lipid while protein decreased. Ash varied little in I- and II-groups after August (2.43-3.90 mg) despite large fluctuations in the other components. The relative amount of ash in I- and II-groups varied between 9%17”/,,.There was a clear inverse relationship between the relative amount of ash and lipid. TN YSA NOESSA

RASCHII

In the O-group there was an increase in wet and dry weights from July to September. During the winter. from September to March, there were decreases in wet

Wet

-0-

weight

-a-O---A--

Dry weight Protein

-.-

Ash

- 80

Lipid

G III

GII

-70

h 0,

-60

,E l-

-50

5

-40

tl 3

-30

L 3

- 20 10

i l

0

W 3

19?6-.+1977

19764-1977 6

O-Group

w

I-Group

p+II-Group

Fig. 2. T/t~~sarloc~s.rcrrmchri: seasonal variations in the mean wet. dry. protem. lipid, and ash weights and 95”~ confidence intervals for 0-. I-, and II-groups; confidence intervals for protein, lipid, and ash for O-group are shown in Table III; the axes are broken between Cl11 and GII; Balstjorden. North Norway.

25 45 22 22

9 10 25 40 12 22 24 23 IO 15 98 7x IO

JulyIY76 Aug. 1976 Sept.1976 Oct. 1976 Nov. 1976 Dec. I976 Jan.1977 Feb.1977 Mar. 1977 Apr. lY77 May 1377 June I977 July1977

5.71 10.79 13.84 9.78 II.85 9.45 9.03 Y.26 8.52 18.91 33.65 33.37 31.60

42.13 53.26 88.62 86.77 79.47 80.83 67.61 69.24 61.12 63.92 53.13 93.01

16 23 26 42 80 Y 61

June 1976 July 1976 Aug. 1976 Sept. 1976 Oct. 1976 Nov. 1976 Dec. IY76 Jan. 1977 Feb. 1977 Mar. 1977 Apr. 1977 June 1Y77

55

65.98 83.90 99.71

48 1 33

1.5Y 3.35 3.83 3.77 4.23 3.88 3.30 3.45 2.70 4.35 12.16 9.00 7.81

I.20 2.31 1.59 I.20 2.66 I.72 1.3Y I.49 1.90 2.39 2.43 I.80 5.51

4.30 4.32 8.75 7.77 3.84 16.63 3.91 7.39 5.18 6.23 5.28 7.09

5.Y9

16.62

8.12 IO.01 21.69 24.92 17.33 22.07 1S.B 16.27 12.58 20.86 13.18 16.03

8.30

27.37

._--.. ..~

9 10 2s 40 12 21 24 23 IO 15 98 76 Y

-

1.03 2,46 2.79 2.00 2.48 2.01 1.77 1.66 1.47 2.46 7.47 7.60 Y.32

9.86 14.50 21.04 23.39 22.65 20.81 17.34 15.70 13.24 12.68 10.47 20.81

25.77

1 32 14 23 25 42 81 Y 57 54 24 46 21 21

14.73

40

u

-

_

0.19 0.89 0.85 0.89 1.10 0.99 0.76 0.71 0.52 0.81 3.58 2.22 3.93

3.20 3.80 6.92 6.14 5.04 5.94 4.52 4.97 3.79 4.54 2.84 4.77

4.02

7.24

SD

and

1-

._~_~

17

10.93

GENERATION1

n

GENERATION 111 0.14 0.63 0.35 8 1.32* 0.28 7 1.00* 0.69 0.45 0.32 4 0.81' 0.31 2 0.X2* 0.37 I 0.83* 0.45 2 I.541 0.72 Y 3.8Y 0.51 6 3.44 2.91 7 3.36

GENERATION11 1.84 7 4.17 1.64 7 6.02 2.85 7 10.40 1.90 15 X.60 1.11 23 8.58 4.48 8 8.70 1.16 Y 6.73 1.34 I1 7.81 1.54 9 6.17 1.35 15 6.42 I29 4 4.08 2.15 4 7.27

1.42

4.66

CD ~~..

0.21) 0.16

0.37 0.78 0.76 I I8 0.95 0.65

0.27 0.26 0.25 1.57 0.95 0.73

1.25 0.68 1.51 1.12 0.57 1.56 1.40 1.42 1.01 0.76 0.71 O.Y4

0.65

CD

~__

0.36 0.42

2.14 1.34 1.39 0.51 0.68

I.%6

1.40 0.90 1.69 2.04 1.33 I.92

I.28

__-

SD

Protein

*, pooled

7 6

13 20 6 8 Y 7 5 3 4

7

6

8

13

n

numbers

1.00 1.01 0.70 0.35

0.29 0.53

0.21 0.1X 0.51% 0.37* 0.38* 0.71* 4.03 4.1I 2.79

0.33 0.86 0.38 0.3Y

0.13 0.35

0.15 0.30

1.45 0.76 2.45 1.53 0.94 I.13 2.54 2.70 1.06 0.40 1.39 I).')6

0.82

CD

3 3

0.51 1.24

0.26 0.38 0.55 0.35 0.39 0.40 0.33 0.36

1.90 2.30 1.96 1.84 3.19

2 6 3 4 I

2 3 4 6 3 3 4 4

2.17 3.19 2.94 2.74

2.16

0.13 0.07

0.00 0.18 0.21 0.11 0.08 0.15 0.11 0.11

0.24 0.13

0.00 0.34 0.29 0.11 0.15 0.27 0.15 0.15

2.37 0.45 0.82 I.13

0.78 0.45 0.45 0.81

1.15

CD

SD,

1.68 I.88 1.06 0.30

;

0.92 1.02 0.58 0.30

0.63

SD

Ash

.U, mean

3 3 3 h

3

x

of individuals;

0.79* 0.68*

1.77 1.03 2.75 2.55 2.02 1.13 2.74 3.59 1.81 0.35 0.76 0.69

1.37

SD -

Lipid -

n,

3.80 5.53 9.53 X.06 7.81 9.19 7.61 6.67 6.59 6.61 5.96 3.71

8.33

-P

(mg);

samples.

and ash weight

limit;

lipid content,

CD, 95”:, confidence

protein

deviation;

Dry weight

standard

of wet and dry weights,

CD

means

Wet weight

monthly

May 1976 June 1976 July1976

Date

Tlt):ranoessa ruschii:

TABLE III

ECO-BIOCHEMISTRY

OF EUPHAUSIIDS

111

weight (13.84-8.52 mg), dry weight (2.79-1.47 mg), protein (1.32-0.83 mg), and lipid (0.79-0.38 mg) whilst ash was more stable varying between 0.33-0.55 mg. Protein was the dominant biochemical component during winter accounting for 42-57x of body dry weight, while lipid varied between 24 and 305)/,.The results from the two sampling dates in October are also shown separately for T. ruschii. A similar change in protein/lipid ratio to that found for T. inermis is seen in T. raschii. The relative amount of ash decreased from 26 to lSoi, between July and March. In the I-group there was a rapid increase in all quantities from March-April to August-September. A possibly less intense growth period during mid-summer, similar to that for T. inermis, can also be seen for T. raschii. From April to August there were increases in wet weight of 3690< (18.91-88.62 mg), in dry weight of 755’:,,, (2.46-21.04 mg), in protein of 575% (1.54-10.40 mg), in lipid of 1242% (0.71-9.53 mg), and in ash of 525% (0.51-3.19 mg). The relative amount of lipid increased from %26407; and protein decreased from %57-40?~ during this period. In winter, from September to April there were decreases in wet weight (86.77-53. i 5 mg) and dry weight (23.39-10.47 mg). Protein and lipid were stable between August and November (z 8 mg). This was followed by decreases in protein from November to April (8.70-4.08 mg) and in lipid from November to July (9.19-3.71 mg). These two biochemical components had similar weight levels in the I-group. In the II-group wet and dry weights, and protein content increased from April to June, while no increase could be seen for lipid. An increase in lipid from June to July can, however, be seen in the IT-group for GII (Table III). The relative amount of lipid decreased from 51-24% and protein increased from 3648% between April and June. In the I- and II-groups ash underwent a slight decrease from x 3 to 2 mg. The relative amount of ash showed maxima in August (17%) and March (2Oy{) and a minimum in October.

The population structure of M. norvegica is unstable (Falk-Petersen & Hopkins, in press) and the O-group did not recruit to the sampled population before November. This group can only, therefore, be followed from November to March, during which time there was a very slight increase in the quantities. The relative amount of protein and lipid decreased between December and February. The lipid content continued to decrease to a minimum (=309;/) in July, while protein increased between May and June ( = 35- = 40”/). Examination of the weight increase in the I-group was not easy because of difficulties in separating GI and GII between September and November. The I-group can be followed from April to June and from January to March. From March to June therewereincreasesin wet weight (167.5-209.0 mg) and dry weight (33.2650.38 mg> whilst protein and lipid were about equal (varying between 16 and 21 mg).

112

The

STIG FALK-PETERSEN

relative

between

amount

of both

protein

(36-23”:))

and

lipid

(477309,;)

decreased

April and June.

-o-

Wet

weight

--

Dry

weight

-o-

Protein

--A--

Lipid

-*

Ash

700 600

0

500

E " l-

400

5 z

300

=

200

L 3

100

G II

I

N'D'J'F'M'A'M'J'J"J

L

I 1 I I 1 J

A

S

1976-1977

t-0-GroupcCt----

0

N'D

J

0

F'M'A'M'J'J'

1976-1977

I-Group

---+11-Group

Fig. 3. M~,~any~/ipha/7c,.v mrvc,~irtr: seasonal variationsin the mean wet, dry. protein, lipid. and ash weights and 95;; confidence intervals for 0-, I-. and II-groups; confidence intervals for protein, lipid. and ash for O-group are shown in Table IV; the axes are broken between GIll and Gil; Balsfjorden. North Norway.

In the II-group there were small changes in wet (z 700 mg) and dry ( z 170 mg) weights from April to July. There was a marked change in the protein;‘lipid ratio between April and May, with protein increasing from x40 mg to z 70 mg and lipid decreasing from x 70 to 55 mg. In the I- and II-groups ash varied x 157: of body dry weight.

625.5

631.2

88.0

26

I

I

1976

1976

1976

July

Aug.

May

I2

1

7

6

4

8

6

1977

I977

1977

lY77

1977

1977

lY76

IY76

1977

1Y77

1Y77

IS77

1977

Mar.

Apr

May

June

July

Oct.

Nov.

Jan. 1977

1977

Feb.

Feb.

Mar.

Apr.

May

June

July

so.5

80.3

126.7

6Y2.0

662.3

4

14

IO

5

38.38

ih.Y4

20Y.0

5135

65.37

49.39

69.53

65.37

45.01

X5.50

213.6

146.1

167.5

37.49

34.6Y

38.84

63.83

26.91

140.2

146.5

34.69

139.4

II.46

4

13

6

7

IO

4

6

2

5

92.9

107.1

1

‘13.2

721.4

18

55.9

I

I2

5

5

4

5

5

6

3

4

II

7

3

50.38

12.42

26.70

6.90

2

4

2

15.54

I s.94 I I .42

30. I7

I

I

46.8

3

11.90 18.74

3

7.51 1024

I 4

8.18

GENEKATION

8.40

15.58

14.14

13.6’)

35.64

17.46

16.35

39.21

39.38

29.6Y

7.99

6.59

GENERATION

11 .hY

24.35

71.62

16.88

II GENERATION

14.92

CD

33.26

32.10

7.37

7.51

31.55 33.07

2.69

23.70

14.70

I

7.31

31.47

170.9 162.4

28.59

30.17

43.64

174.9

173.2

21 IX

171.5

179.1

I2 8

197.1 27.74

39.2 40.46

161.7

53.5

78.6

47.18 43.97

6

19X.1

170.‘)

26

62.5

113.0

125.1

684.2

704.9

18

742.1

22

173.3

54.2

103.5

161.4

130.1

133,‘)

136.9

114.7

182.3

161.4

569.0

685.9

?I

X

6

27

IY76

Nov

Jan. 1977

7 7

12

652.7

Ott

656.6

1976

lY76

Sept.

63.0

I

263.7

I

5.75

1976

4.74

25.3

36.5

37 7 _“._

28.94

34.56

25.98

SD

27.0

1

136.0

160.X

146.5

145.5

.\

weight

4

Aug.

11

26

42.04

1

IO

14

II

Dry

4

155.7

5

1976

July

119.9

4

June lY76

TABLE IV

IY.2’)

21.38

16.23

17.10

17.79

13.93

14.36

10.14

X.84

2.34

0.08

4.32

2.24

5.79

9.74

12.99

65.88 72.94

11.29

x.34

14.49

7.95

77.14

41 79

47.55

55.96

17.03 12.24

14 87

3.55

36.88

3,24

0,24

7.93

4.1 I

8.05

13.54

14.93

1 I.29

8 34

26.60

10.55

8.12

iY.57

14.87

6.52

X.89

I

14.1

19.16

CD

16.71

64.58

III

II

1

SD

66.25

71.52

16.74

56.10

62.98

57.Y4

i

Protzin

15.79 17.70

1

16.19

lX.Y9

9.88

5 7’)

693

54.54

61.35

52.32

72.83

3

2

3

2

5

I

4

4

5

5

61.98

x3.02

3 i

XI IO

59.87

X.92

10.54

3h.7Y

5Y.52

33.45

5

5

h

1

1

IO

6

of wet and dry weights, protein and lipid content. and ash weight SD.standard deviation; CD. 95”, confidence limit. -

Y6. I’)

65.47

CD

means

29. I

32.3

104.3

134.6

108.7

SD

weight

monthly

44.Y

622 I

I0

June 1976

678.6

.x

Wet

14

,I

---

mrt~~~i~u:

1976

May

Date

M~,~u,1?,~tiphrr/7e~

10.31

11.00

2.01

0 00

3.6Y

I Y.4Y

lg.‘)2

0.91

6.41

3.53 2 77

3.06

21.28

15.31

1732

15.07

17.85

15 50

22.19 12.x4

iY.12

61.78 21.31

33.65

x.2x 20.53

7.20

32 67

I?.%+

13.76

17 86

12.67

19.40

13.76

Liptci

(mg); H. numbers

2

4

3

c!

3

3

1

2

I

3

I

3

I

3

6.80

20.35

‘5.92

28 27

24.47

14.4’)

25.99

19.29

X.48

11.75

21.16

17.53

17.41

22.16

1 36

SD

4.68

4.58

3.95

7.15

Y.25

1.10

4.30

9.50

IO.13

14 23

6.37

7.25

21.71

16.Y8

2.02

5.98

XX8

18.60

X.80

2.50

CD

7. mean;

4.80

Ash

of individuals:

114

STIG FALK-PETERSEN

DISCUSSION

In Balsfjorden primary production peaks can be seen in April and AugustSeptember whilst the summer minimum lasts from May to July (Falk-Petersen & Hopkins, in press). In the present study Thysanoessa inermis and T. raschii rapidly increased in weight from April to September-October, except for a possibly less intense weight increase during midsummer corresponding to the summer minimum primary production. The I-group started their weight increase in March, whilst the II-group began to increase in weight in April-May. The onset of growth shows the same trend as found for the length increase (Falk-Petersen & Hopkins, in press) a-nd can possibly be associated with the phytoplankton succession. The small algae Phaeocystispouchetii (Hariot) Lagerheim underwent a mass increase in late March, whilst the larger diatoms dominated in late April. During winter, O-group Thysanoessa inermis and T. raschii showed no weight increases, and in the latter case there was a slight decrease in the mean weight. For I-group T. inermis and T. raschii the decreases in weight during winter can partly be explained by a decrease in the mean carapace length (see Falk-Petersen & Hopkins, in press). The variations in the biochemical composition of euphausiids in Balsfjorden also appear to be related to the primary production cycle. During growth periods there were increases in both protein and lipid, lipid increasing relatively more than protein in both T. jnerrn~.~and T. ras~~j~. Lipid decreased from November to February in the case of O-group T. inermis while O-group T. raschii showed a decrease in lipid between January and February. This change in the protein/lipid ratio is not only related to the low phytoplankton standing stock, but may also be due to a fall in food quality as evidenced by high C/N values of the particulate matter after December (Eilertsen, 1979). O-group Thysanuessa probably use their energy reserves built up during summer to maintain their basic metabolism until the onset of the spring phytoplankton bloom in March. The production of gonads is normally an energy-demanding process with active mobilization and synthesis of organic components (Giese & Araki, 1962; Pillay & McNair, 1973). Since zooplankton from high latitudes appear to spawn lipid-rich eggs (Benson & Lee, 1975; Lee, 1975; Bamstedt & Matthews, 1976) there is probably “‘stress” on the animal’s lipid reserves to build up gonads and to spawn. The marked decrease in the relative amount of lipid in T. inermis and ~egan~v~ti~hane.~norvegica I-group after January may be associated with use of energy due to over-wintering and mobilization of energy reserves for growth of gonads. The pronounced decrease in both the relative and actual quantities of lipid in Thysanoessa inermis I-group is also “real” at the individual level and coincides in time with transference of spermatophores and spawning (Falk-Petersen & Hopkins, 1979). In T. raschii I-group, however, there is no decrease in the relative amount of lipid during winter; protein and lipid decrease with decreasing dry weight. Differences in the lipid content in I-group T. inermis and T. ras~~~~~ in the winter also appear to indicate

ECO-BIOCHEMISTRY

OF EUPHAUSIIDS

115

different metabolic or physiological responses towards over-wintering. Since Meganyctiphanes norvegica is not maintained as a stable population in Balsfjorden (Falk-Petersen & Hopkins, in press), a discussion of the dynamics of the variations in the quantities is difficult. There were small changes in wet and dry weights in the 0- and I-groups from November to July (GIII), and in the I-groups from December to July (GII). The increase in weight in I-group from July to December could be due to both growth as well as recruitment from other populations outside the fjord. The pronounced increase in protein from April to May in II-group occurs at the same time as the spring phytoplankton bloom. The proportion of protein and ash is higher and lipid lower in the O-groups than in I- and II-groups in euphausiids from Balsfjorden (see Table II). For Thysunoessa inermis an increase in the proportion of ash appears to be associated with a decrease in lipid, while no such trend can be seen for T. raschiiand Meganyctiphanes norvegica.

Conover (1964) has discussed the growth of filter-feeding zooplankton and has demonstrated, for C~~~~~~~~ ~l~~er~orea.~, that during periods of weight increase most of the increase is due to the building-up of energy-rich lipid reserves (R 10000 cal . g-‘). The food during this period (mainly phytoplankton) has, however, a calorific value of = 5500 cal . g- ‘. In Balsfjorden, the two Thysanocssa species, which are mainly herbivores, show a relatively larger increase in lipid than in protein content during the primary production period. Lipid must, therefore. also be synthesized from lower or less concentrated energy sources, such as protein in the diet. The rapid weight increase and even more exceptional increase in lipid for T. ~~?e~~~s and T. rasctz~jshows that these species ingest food effectively and also possess an efficient lipid-synthesizing system which can convert a diet (mainly phytoplankton) with an energy content of ~5500 cal .g-’ to lipid of energy content = 10000 cal ag-.‘. The growth potential and the ability to synthesize high energy storage products must play an important role in the over-wintering biology of these euphausiids. variables such as geographical and vertical distribution, similarity in relative abundance, and food and feeding methods have been used to examine niche divergence. Biochemical composition can also prove to be a useful tool in the examination of ecological niches. Lee (1974) showed that zooplankton from Bute Inlet, B.C., Canada, could be divided into two categories based on biochemical criteria; those that turned excess food into storage lipid and those that used most of the food for forming new tissues. Since protein is assumed not to have a storage function, it can be assumed that zooplankton with low lipid levels require to feed constantly. Clarke (1977) suggested that Euphausia superha must feed over-winter because it has relatively low levels of storage lipid (mainly triacylglycerol). It is suggested that during the winter months E. superba switches to a more omnivorous diet. In contrast, E. cr~~stalforop~~ius, a species which has high levels of storage lipid (mainly wax esters) seems to be able to over-winter without feeding. In Bals~orden

116

ECO-BIOCHEMISTRY

60 r

-0-

Protein

--A--

Lipid

-.-

Ash

117

OF EUPHAUS11DS

Thysanoessa

inermis

G II

m-m

/

1.

m&m_./-•

Thysanoessa

raschii

Meganyc tiphanes

O-

II

G II

norvcgica

_-_--__

J~‘~~~‘I,‘j’~‘~‘~‘~‘J’J”~‘J’~‘S’b’~’b’J’F’M’A’M’J’J1

l-

Fig. 4. 7%pmoessa inermi.s, T. mschii. and Mqunycr@mc~ c~~vrgicn : seasonal variations in protein. lipid. and ash as percentage of dry body weight for 0-, I-, and II-groups: the axes are broken between GIII and Gff; &&ijorden, North Norway.

118

STIG FALK-PETERSEN

I-group T/z~sc~~~oe.sssu inrrmis has relatively high lipid levels (‘2:48%) in contrast to T. raschii and Meganyctiphanes norvegica which have z 37”/, (Table V). Preliminary analyses of the lipid extracts show that Thysanoessa inermis has wax esters as a major lipid depot, whilst T. raschii and Megaryctiphanes norvegica have triacylglycerols (Sargent, pers. comm.). This indicates that the last two species probabiy switch to a more omnivorous diet during winter, while T. j~~~r~zi.~ is a more “obligate” herbivore. The ilnportance of lipid in Arctic plankton was emphasized by Sheard (1953). The hypothesis that zooplankton from high latitudes has a higher lipid content than zooplankton from low latitudes has been supported by several authors (Lee et al., 1972; Ferguson & Raymont, 1974; Lee, 1974; Benson & Lee, 1975). The biochemical compositions of Thysanoessa inermis, T. raschii, and Meganyctiphanes norvegica from different geographical regions, ranging from 50 to 70”N, are compared in Table V. The lipid content is considerably higher in the euphausiids from the subarctic Bals~orden than from the temperate-bor~l waters. This further supports the concept that lipid is especially important in the ecology of zooplankton from high latitudes. The difference in lipid levels in zooplankton from different latitudes reflects the difference in light climate and its influence on primary production. To survive in polar waters herbivorous zooplankton must, therefore, synthesize large lipid stores during the primary production period, and use them for maintenance over-winter (Clarke, 1977). ACKNOWLEDGEMENTS

I am indebted to Dr. C. C. E. Hopkins for guidance during this work, and to both him and Dr. J. Sargent for critical reading of the manuscript. I also thank the ships complement of R. Y. &as, R. V. Asterias and R. V, Johan Ruud and our technicians for assistance and willing co-operation. This work was supported in part by the Norwegian Fisheries Research Council (NFFR); project no. 401.04 and 401.09. REFERENCES G. T.. 1978. fk mtarcric h-rill wsoww: pzwprcts,f& comnwrcial ~~.~pi#ituti~r~. Tetra Tech. inc.. California. 144 pp. B.AMSTFDI, U., 1975. Studies on the deep-water pelagic community of Korsfjorden, western Norway. Ecological aspects of individual variation in weight and protein and lipid content of Euchaua norwgica (Copepoda). Sursia, Vol. 59, pp. 31-46. BKMSTFWT, U., 1976. Studies on the deep-water pelagic community of Korsfjorden, western Norway. Changes in the size and biochemical composition of Mqanyctiphanes norvegica (Euphausiacea) in relation to its life cycle. Sarsiu, Vol. 61, pp. 15-30. B&STFDT, U.. 1978. Studies on the deep-water pelagic community of Korsfjorden, western Norway. Seasonal variation in weight and biochemical composition of Cfririks armatrfs (Copepoda). Bowomvsis arctica (Mysidacea). and Ezi~r#h~~a ~7~~~7ff~u (Cha~to~natha~ in relation to their biology. Sarsia, Vol. 63, pp. 145-154. B,~~~Kus.

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