Continental She~Research, Vol. 8, No. 4, pp. 329-345, 1988. 0278-4343/88 $3.00 + 0.00 Printed in Great Britain. © 1988 Pergamon Press plc.

F o o d - l i m i t e d g r o w t h o f Euphausia superba in A d m i r a l t y Bay , S o u t h S h e t l a n d I s lands , Antarc t i ca

S. MCCLATCHIE*

(Received 14 May 1987; accepted 16 September 1987)

Abstract--Length-frequency data for Euphausia superba and chlorophyll a concentrations from Admiralty Bay, South Shetland Islands, Antarctica over 1 year were used to test the hypothesis that kriU growth is limited by food concentration. Growth rates calculated using the ELEFAN computer program yielded values comparable with laboratory rates, but gave slow positive growth rather than negative or zero growth during winter. Seasonal growth rates closely followed water column pigment concentration, and indicated that both krill age class and food concen- tration should be included in models of krill growth. Growth rate of Group 0, I and II age classes was a hyperbolic function of food concentration. Maximum growth rates varied with age class and occurred only at concentrations greater than about 50 p.g Chl a m -2. Age class specific thresholds

2 for zero srowth occurred at water column concentrations of 9.2-17.5 I~g Chl a m- or 0.06-0.1 ~tg Chl a l -~ with homogeneous pigment concentration. Negative growth is expected at concen- trations below these thresholds. The analysis demonstrates that krill growth was food limited for six months of the year, but also shows that krill can often meet their minimum requirements for growth at the low concentrations of phytoplankton characterizing offshore Southern Ocean waters.

INTRODUCTION

IT HAS generally been assumed that the growth of euphausiids varies seasonally as a function of temperature and food supply if all other factors, such as reproductive state, are equal (MAUCHLINE and FISHER, 1969). Population growth curves for temperate and polar euphausiid species are typically step-like, due to increased rates of growth in spring and summer when food is more abundant and temperatures are warmer than in winter when food is scarce (EINARSSON, 1945; MAUCHLINE and FISHER, 1969). Growth curves of E. superba characteristically show accelerated growth in spring (RUUD, 1932; FRASER, 1936; BARGMANN, 1945; MACKINTOSH, 1972, and others). This has been assumed to be related to the vernal increase of phytoplankton abundance. Although food limitation of growth in euphausiids is deduced from indirect evidence (HOLM-HANSEN and HUNTLEY, 1984) or demonstrated in the laboratory (IKEDA and THOMAS, in press), an empirical analysis has not been made of krill population growth in relation to their food in the field. MACKINTOSH (1972) presented HART'S (1942) data on phytoplankton pigment units in conjunction with his growth curves which were compiled from length-frequency data from the R.R.S. Discovery expedition samples from 1927 to 1965 for separate regions. The qualitative relationship between growth rate of Euphausia superba and the seasonal cycle of phytoplankton abundance suggested that an hypothesis of food-limited growth

* Portobello Marine Laboratory, University of Otago, P.O. Box 8, Portobello, New Zealand.

329

330 S. MCCLATCHIE

may be valid. However he noted that in some instances the acceleration of krill growth occurred before the seasonal phytoplankton increase and suggested either that krill growth was greatly affected by small increases in phytoplankton abundance, or that krill were supplementing their diet with animal food (MAcm~'rOSH, 1972). Food supply is an integral part of models attempting to describe the population growth of E. superba (ASTHEIMER et al., 1985; ASTHEIMER, 1986), but empirical data are lacking.

MACKINTOSH (1972) distinguished between krill population growth, apparent popula- tion growth, and individual krill growth, emphasizing that they are not necessarily the same. Population growth is difficult to measure because populations move with the hydrographic regime (HEYWOOD et al., 1985), and may travel large distances on seasonal time scales (MACKINTOSH, 1972). Individual growth of adults and larvae can be measured by growing the krill in the laboratory (IKEDA and DIXON, 1982; IKEDA, 1984, 1985), or estimated from molt increments and intermolt periods (MAUCHLINE, 1980). Laboratory growth rates can be measured accurately, but it is difficult to ascertain whether conditions for growth are representative of the field. There are no laboratory studies where the abundance of food was varied on a seasonal basis.

There are very few instances where local apparent growth of any euphausiid species and the abundance of their associated food organisms were measured over a year or longer. As well as the published data set for Meganyctiphanes norvegica in the Kattegat (BOVSEN and BUCHHOLZ, 1984), data are available for E. superba in Admiralty Bay, a fiord on King George Island, South Shetland Islands, Antarctica (62°8'S, 58°26'W) (Fig. 1). My aim in this. paper is to test the hypothesis that local apparent growth of E. superba was limited by food in Admiralty Bay in 1979. To do this, I examined the relationship between the local apparent growth rate of E. superba and the seasonal concentration of phytoplankton pigment (Chl a) in Admiralty Bay. Krill growth rate was calculated from the time-series of length-frequency data (STEPNIK, 1982), and phyto- plankton abundance from the data of LiPsra (in press).

64eW

61"S.

54"W

"62"00~

64~J •

Fig. 1. 58"28'W

Regional map to show location of Admiralty Bay. Stations 5 and 8 are collection sites for phytoplankton pigments.

Food-limited growth of E. superba 331

Krill growth rates were calculated using the Electronic Length Frequency Analysis computer program (ELEFAN). This method was used rather than the Petersen method or Modal Class Progression Analysis for the reasons outlined in PAULV and DAVID (1981). Basically, these earlier methods may produce questionable results where the spawning season is long or occurs in several batches so that the peaks in a time-series of length-frequency distributions may not represent discrete year classes (PAULY and DAVID, 1981). In such cases the peaks of any given sample cannot be unequivocably connected with the peaks of preceding or successive samples. The ELEFAN program purports to use an objective method for evaluating growth parameters which overcomes the subjective interpretation of modes in length-frequency data (PAuLY and DAVlO, 1981). Previous analyses of krill length-frequency data have generally used the progres- sion of mean length to estimate growth rates (FALK-PETERSEN and HOPKINS, 1981; ETIXRSHANK, 1983; BUCHHOLZ, 1983; BOYSEN and BUCHHOLZ, 1984). All of these studies suffer from the subjective interpretation of length-frequency data. The computer program also has subjective elements in the choice of optimization methods used, but has the advantage that different investigators should arrive at the same answer for a given data set.

A fundamental assumption in the analysis of local apparent growth is that krill of the same age are the same length. This is a potential source of error because in the laboratory E. superba decrease in size when food is absent or inadequate (IKEDA and DIXON, 1982). If shrinkage occurs in the field it should result in a blurring of the age-class structure of the population, making the estimation of growth rate more difficult. ETI~RSHANK (1983) argued that for this reason it is impossible to estimate the population growth of krill using length-frequency methods. However, it has not yet been determined to what degree the size structure of a population would be obscured by shrinkage of kriU in winter. The effect of shrinkage on population structure would be further compounded if shrinkage is size- related, larger krill showing negative growth at high food concentrations than smaller krill. It is also not certain that negative growth occurs in all regions of the Southern Ocean, particularly in warmer zones such as the South Shetland Islands.

Local apparent growth, derived from analysis of length-frequency distributions of field samples, may approach population growth in areas with a localized hydrographic regime, such as fiords. MACI<INTOSH (1972) notes that "the pattern of local apparent growth is clearest in the Bransfield Strait or Northern Weddell Drift where the size of the area or water conditions within it do not allow for large geographical variations". For this reason, the krill populations in the fiords of the South Shetland Islands are particularly well suited for a study of local apparent growth.

ADMIRALTY BAY

PRUSZAK (1980) suggests that a two-phase circulation typical of fiords occurs in Admiralty Bay. There is an inflow of water from Bransfield Strait at the bottom, and an outflow of water into Bransfield Strait at the surface (PRUSZAK, 1980; RAKUSA-SUSZC- ZEWSKI, 1980). Tidal forcing is the main cause of water mixing between Admiralty Bay and the Bransfield Strait (RAKusA-SuszczEWSKI, 1980). Drift surface currents reaching to a depth of only a few meters and generated by the wind field are superimposed on the two-phase current system driven by the tides. According to PRUSZAK (1980), surface circulation in Admiralty Bay is dependent upon wind direction for wind speeds

332 s. MCCLATCHIE

5-

P E @ I-

4 ¸

3.

2,

1-

O,

-1

- 2 32 .5

Q SSSW

• o e o •

eee

• . ." BS ." WWWS

•

AP

• " 50m 200m WDW AB AB

3'3 3~.5 s'4 3;.s 3s $1111nit y %0

Fig. 2. Water mass characteristics of Admiralty Bay (AB). Dots are surface water values, hatched boxes are extreme values at 50 and 200 m, from SZAratANSKI and LIPSKI (1982). Ellipses are from STEIN (1983); BS, Bellingshausen Sea; DP, Drake Passage; AP, Antarctic Penninsula shelf; SSSW, surface Scotia Sea water; WWWS, winter Weddell Sea water; WDW, Warm Deep

Water.

exceeding 4 m s -1. The mean wind speed for summer months is 7 m s -1. At wind speeds exceeding 10 m s -1 the pattern of surface currents is disrupted by violent gusts and a spatially and temporally heterogeneous and unstable wind field. Wind forcing dominates any effect of tides on the surface currents which flow in the same direction as the wind, except when wind speed falls below 3 m s -1.

PROSZAK (1980) estimated that in the upper 100 m of the water column the time scale for exchange of waters between Admiralty Bay and the Bransfield Strait is 1-2 weeks. This suggests that the krill population of Admiralty Bay is not distinct from that of the Bransfield Strait, although at times the population structures in the two regions appear to differ (RAzUSA-SUSzCZ~WSra, personal communication).

Temperature and salinity data for summer 1978-1979 from SZAFgANSKt and LIPSIa (1982) were used to characterize the water masses in Admiralty Bay. Surface tempera- tures and salinities were variable, with characteristics of Bellingshausen Sea and Drake Passage waters as described by STEIN (1983). Water from 50 m depth had characteristics very similar to the temperature and salinity of Bellingshausen Sea water reported by SatIN (1983) (Fig. 2). The salinity distribution of water from Admiralty Bay is consistent with origins in the Bellingshausen Sea or Antarctic Penninsula shelf waters (cf. STEI~q, 1983), although the summer water temperatures were warmer.

METHODS

E. superba were collected by STEPNIK (1982) using a 2 x 1 m mouth size trawl, with 6 mm mesh in the front and 60 pm mesh in the rear of the net. The trawl was fished from 100 m to the surface for approximately 20 min at about 0.8 m s -1. Samples were collected in Admiralty Bay and Ezcurra Inlet in the vicinity of Arctowski Station.

Food-limited growth of E. s u p e r b a 333

STEPNIK (1982) reported that a total of 250 trawl samples were collected, and 150 krill measured to the nearest mm from each sample. Samples from the same month were pooled. As the winter of 1979 was exceptionally mild, Admiralty Bay did not freeze over, and year-round collection of samples was possible (STEPmK, 1982).

Average growth curves for male and female E. superba were estimated from the January to December 1979 length-frequency histograms in Sa~PNIK (1982, his Fig. 3). Although sex-related differences in growth rate occur in Thysanoessa longipes (NEMOTO, 1957), differences are less marked in other species (MAUCnLIN-Z and FISHER, 1969), SO that calculating an average combined growth curve for the sexes is justifiable. Growth curves were derived by fitting a modified Von Bertalanffy growth function (hereafter VBGF), often used in fisheries biology, to the data using the ELEFAN program. ELEFAN calculates a multitude of growth curves from a series of length-frequency samples sequentially arranged in time, and selects the single curve which passes through the maximum number of peaks (PAULY and DAVID, 1981). The assumptions made in applying this procedure are (1) that the time series of samples represent the same population and are representative of the population; (2) that the growth pattern of the population is the same from year to year; (3) that the VBGF describes the average growth of the population, and (4) that differences in length can be attributed to differences in age (PAULY a n d DAVID, 1981).

The VBGF represents in integral form the balance between anabolic and catabolic physiological processes. Anabolism is assumed proportional to surface area and catabo- lism is assumed proportional to weight (PAULY, 1979). The specialized VBGF assumes that both surface area and body weight increase isometrically as length increases:

Lt = Loo • ( 1 - e-r(t--t°)) 3, (1)

where Lt is krill length at time t, Loo is the asymptotic length which an average krill would attain, and to is the time from which the VBGF describes the growth pattern. K is a "stress factor", proportional to the rate of catabolism (PAULY, 1979). Since growth is usually allometric, the generalized VBGF is more appropriate:

L t = Loo • (1 - e - 3 D / b " r ( t - t o ) ) b / O (2)

D = b - a, where b and a are the exponents relating length to weight and surface area, having values of b = 3 and a = 2 in the isometric case.

ELEFAN uses an optimization procedure to fit four parameters (L~, K, W P and C) to a generalized VBGF incorporating seasonal fluctuations in growth:

L t = L®(1 - e -[k" D ( t - to) + C . K . D/2n . sin 2n (t - ts)l) l / D ' (3)

where ts + 0.5 = WP, the Winter Point, which corresponds to the month of the year when growth is slowest, ts is defined as the start of the first oscillation with respect to to, and C is a dimensionless constant which expresses the intensity of the seasonal growth oscillations. The best growth curve describing the data was selected by varying the parameters of the VBGF (PAULV and DAVID, 1981).

The optimization process used by ELEFAN is sensitive to the selection of seed values for the parameters L®, K, C, and WP, so that the recommendations of PAtSLV et al. (1980) were followed. W P was set to 0.6, corresponding to minimum growth in June, and L® was set to 66 mm. The value of C was set to 0.5 corresponding to a maximum estimated seasonal difference in water temperature of 5°C. The initial value of K was

334 S. MCCLATCttlE

chosen to generate a reasonable life span, such that K • life span ~ 3 when D = 1 (PAULY et al., 1980). K was adjusted upward slightly during the optimization runs when a value of D = 0.9 produced a better fit.

The size selectivity of STEPNIK'S (1982) trawl was determined using a length-converted catch curve (PAuLY, 1983). Gear selectivity could seriously bias the population structure of the samples, and any growth curves derived from them. After determining the gear selectivity, the predicted growth curves were compared to laboratory data on larval growth rates (IKEDA, 1984) to assess whether the growth curves were accurate over the size range of krill that was poorly sampled by the trawl. Total krill mortality was estimated from the length-converted catch curve (PAuLY, 1983, 1984a,b).

The relationship between krill growth rate and depth-integrated pigment concen- tration was described using a modified Ivlev equation (fitted by Marquardt procedure):

G = Gmax(1 - e -'Q(p - P')), (4)

where G is krill growth rate (mm day- i ) , Gma~ is the asymtotic growth rate, and u is the initial slope, p is food concentration (mg Chl a m-2), and p ' is a threshold food concentration for zero growth. The threshold concentration was incorporated to allow for IKEDA and DIXON'S (1982) observations that E. superba shrinks when starved in the laboratory. One large positive growth rate (out of a total of 45 rates) was excluded from the data. No test of significance was applied because F-tests are invalid for non-linear curve fitting (DRAPER and SMrrH, 1981).

RESULTS

The ELEFAN growth curve calculated for STEPNIK'S (1982) data (Fig. 3) predicts a krill length of 0.85 mm on 15 March (Fig. 4). Larvae of this size would be half way through the Nauplius II stage and approximately 16 days old (IKEDA, 1984), giving a spawning date of 28 February. This is a reasonable date for the start of a mean growth curve in Admiralty Bay, since Ross and QUETIN (1983) reported spawning E. superba around the south Sheltand Islands on 13--14 February 1982. If 35 mm E. superba are assumed to be mature (IKEDA, 1985), krill would reach maturity 486 days after hatching

6 0

=; s o =. :r 4 0

2 0 .

10

0 ~

,, ® ® ® ,~ ® ® - , ® ® ® ~ ~ y,

Fig. 3. Length-frequency data for E. superba in Admiralty Bay from STEPNIK (1982) with superimposed ELEFAN growth curve.

Food-limited growth of E. superba 335

6 0

50-

40- E E

30- C !

.~ 20-

1 0

,o,.O.'"

/ ...."

lllllo ..... /""""'" /

o 5~o 1~oo days since hatching

1500

Fig. 4. Comparison of life-cycle growth curves for E. superba, adjusted to the 28 February hatching date estimated by ELEFAN. - - ELEFAN growth curve; . . . . . . . ASTHEIMER'S (1985) PPF(S1) model; ..... Ir, EDA'S (1985) maximum growth curve; • • • IKEDA'S (1984) larval growth

data.

in Admiralty Bay according to the ELEFAN growth curve (Fig. 4). The life-cycle curve derived from the local apparent growth of E. superba in Admiralty Bay (Fig. 4) suggests krill live about 4 years in this fiord.

Probability of capture derived from a length-converted catch curve indicates that E. superba larger than 33 mm were efficiently sampled by the trawl (Table 1) indicating adult krill were adequately sampled. The mean length at first capture was 28.2 mm. The length-converted catch curve allows total mortality to be estimated from the descending right arm of the curve (Fig. 5). The convex shape indicates that total mortality was not constant, but increases with size or age. A single value for total mortality cannot be calculated for a curve of this type, which resembles length-converted catch curves typical of anchovies (PAULY, 1984b). Increasing mortality with size could arise from increased vulnerability of larger krill to predators such as seabirds or seals.

Table 1. Probability of capture estimated from length-converted catch curve for the trawl gear used by STEeNII~ (1982) to obtain krill length-frequency data

Mid-length Number Number Probability (mm) caught available of capture

15 2 637 0.0031 17 1 542 0.0018 19 6 457 0.013 21 18 384 0.047 23 40 319 0.125 25 63 263 0.240 27 80 214 0.373 29 72 173 0.415 31 92 138 0.665 33 109 109 1.000

336 S. MCCLATCHIE

6-

: ,

c 4-

2-

X X X

X X

X

X

• m m m n ii o []

DQQ

Q I

o • i

o

0 [] o .5

i i i • 1 5 2 2.5 3

(years)

Fig. 5. Length-converted catch curve derived from length-frequency data in STEPNIK (1982). Samples for all 12 months are combined. • Data used for mortality rate estimate, x Constant

mortality rate.

The mean growth curve estimated using ELEFAN indicated rapid growth from December 1978 to May 1979, with decreasing but still positive growth rate over the winter period (June 1979 to October 1979) (Fig. 3). The length-frequency histograms during the months April, June and July show no clear modal value. Mean monthly krill length increases from December 1978 to March 1979, decreases from April to August, and increases again from September 1979 to March 1980 (Ea'TERSHAN~:, 1983). The ELEFAN analysis does not support EnERSHANK'S (1983) interpretation of the changes in mean krill length as evidence for negative growth in the winter. It is equally plausible that the shift to a smaller mean size during winter arose from mortality of larger krill (S. RAKUSA-SUSZCZEWSKI, personal communication). This is supported by the length- converted catch curve which indicates krill mortality increases with increasing size.

Four age classes could be discerned for STEPNIK'S (1982) data (Fig. 6). Group 0 E. superba aged less than i year grew from hatching to 22 mm length in their first year. Group I E. superba aged 1-2 years were between 25 and 44 mm length. Group II krill aged 2-3 years were 46--55 mm length, and Group III krill older than 3 years were 56-- 60 mm long.

The ELEFAN growth curve gave the best fit with a value for K of 0.8 for growth over the entire year. Growth rates were strongly seasonal and dependent on krill size (Fig. 7). Maximal summer growth rates ranged from 0.13 mm day -1 for Group 0 krill to 0.025 mm day -1 for Group III krill. Minimal winter growth rates ranged from 0.048 to 0.01 mm day -1 for Group 0 and Group III krill, respectively. Growth rates of Group 0 krill declined to a greater extent in winter than was the case for the larger Group I, Group II and Group III krill (Fig. 8).

The seasonal growth rate of E. superba (Fig. 8) showed a very similar pattern to the depth-integrated seasonal concentration of Chl a in Admiralty Bay (Fig. 9). Phytoplank-

Food-limited growth of E. superba 337

Fig. 6.

60 |5o 4 0

E 30.

m

20-

10-

0 , ,

J F M A " J J A S b lq D month

Seasonal growth of year classes of E. superba in Admiralty Bay estimated by ELEFAN from date of STEP~K (1982). [] 0 Group; • I Group; O II Group; • III Group.

Fig. 7.

. 15

0 o 1'0 io 3'0 4'0 ~o eo

body length mm

Growth rate of E. superba in Admiralty Bay as a function of krill length showing effect of seasonal oscillations in growth rate.

ton abundance at two stations in Admiralty Bay were very similar, with peak water column concentrations in December and in March-April. Minimum values for water column concentration of pigments were found in July-August. Chlorophyll a concen- trations were low throughout the year, reaching peak values of 1.15-1.3 Ixg 1-1 during February and March in the upper 50 m of the water column (Fig. 10). Chlorophyll a concentrations during the winter were uniformly low (0.09-0.2 ~tg 1-1) and almost evenly distributed in the water column (Fig. 11).

338 S. MCCLATCHIE

. 1 5

Fig. 8.

"o .1

E £

i F -

.05 C~

month

Seasonal growth rates of E. superba age classes in Admiralty Bay showing winter minimum. [] 0 Group; • I Group; (3 II Group; • III Group.

2 0 0

150-

7 E (Ul

"~ I O 0 - U C~ E

50-

J M j j Z S b b month

Fig. 9. Seasonal variation in depth-integrated Chl a (rag m -z) at two stations in Admiralty Bay in 1979 (Ln, srd, unpublished data). [] Station 5 (62°08.7'S; 58"25.1'W), integrated from surface to

400 m; • Station 8 (62"08.8'S; 58~28.9'W), integrated from surface to 230 m.

The seasonality of krill growth rate was stongly related to food supply, as measured by the depth-integrated pigment concentration (Fig. 12). The fitted curves show that each age class had a quantitatively different response to food limitation, although there was insufficient data to fit a curve to the Group III data. Group II krill achieved maximal growth at lower food concentrations than Group I and Group 0 krill. Older krill also showed a less marked change in growth rate with increasing food supply (higher a, Table 2) (Fig. 12). However, the curves suggest that older krill (Group II) exhibit

Food-limited growth of E. superba 339

mg Chl a m 3

0 .2 .4 ,6 .8 1.0 1.2 1.4 o

lOOfj I ' 1 ~ n Nov

• Dec o Jan

300 • Feb AMar

, A p r

4 0 0

Fig. 10. Vertical profiles of mean Chl a concentration (rag m -a) at Stas 5 and 8 in Admiralty Bay during summer months, November-April 1979 (LiPSrd, unpublished data).

o

lO0

E

200- ®

300 -

4O0-

mg Chl a m 3

.2 .4 .6 .8 1.0 1.2 1.4 I I I I I

o May

Jun

o Jul

• Aug • Sep • Oct

Fig. 11. Vertical profiles of mean Chi a concentration (mg m -3) at Stas and 8 in Admiralty Bay during winter months, May-October 1979 (LIPSKI, unpublished data).

negative growth at higher food concentrations than do younger Group I and Group 0 krill (Fig. 12). This indicates that the growth rate of krill is progressively less sensitive to changes in food availability as the animals age, providing that the threshold for zero growth (p') is exceeded. However, older krill are more likely than younger krill to shrink when food concentrations are low.

340 S. MCCLATCHIE

7 'U

E E o m d~

o

.15

.os-4

O-

- . 0 5

o 0 group ~ I group

II group

. . . . . . . : . . . . . . . . .

- .1 i 0 i O 1()0 150 2 0 0

mg Chl a_ m -2

Fig. 12. Growth rate of E. superba as function of average depth-integrated Chl a concentration at Stas 5 and 8. Growth rates for three age groups were derived from ELEFAN. Negative growth rates at zero pigment concentration are from IKEDA and DIxoN (1982). Symbols for age classes are as in Fig. 6. Nonlinear curves are: Y = 0 . 1 2 7 ( 1 - e x p -°'°27(x-9"249)) for Group 0; Y = 0.0836(1 - exp ~ '°28(x- 12.s23)) for Group I; Y = 0.0415(1 - exp -°'°35Cx- 17.524)) for

Group II.

Table 2. Fitted values for modified Ivlev type curves (equation 4) used to describe the relationship between krill growth rate and watercolumn pigment concentration

(Fig. 12)

Age class Gmax ct p '

Group 0 0.127 0.027 9.249 Group I 0.083 0.028 12.523 Group II 0.041 0.035 17.524

D I S C U S S I O N

E. superba is known to be omnivorous (BOYD et al., 1984; PRICE et al., in press) but its functional morphology (NEMOTO, 1967; MCCLATCHIE and BOYD, 1983), grazing rates on phytoplankton (ANTEZANA et al . , 1982; BOYD et al., 1984), and fecal pellet contents (MARCHANT and NASH, 1986; TANOUE and HARA, 1986) indicate that phytoplankton larger than 5 ~tm are important food. Size fractionation of phytoplankton has shown that, with some regional exceptions, picoplankton (<2 Ixm) contribute little to pigment concentration, and nanoplankton (2-20 l~m) constitute the bulk (up to 80%) of the biomass in the Southern Ocean (WEBER and EL SAYED, 1986). Seasonal variation in plant pigments in the water column was assumed to be an indicator of the nanoplankton and net plankton (>20 ~tm) food concentration available to E. superba in Admiralty Bay. These components of E. superba's diet were used as an indicator of seasonal food abundance, rather than representing the total food available.

Bias of the krill population structure may have arisen from gear selectivity of the trawl used to collect the samples. One independent way to check for this bias is to compare the

Food-limited growth of E. superba 341

ELEFAN growth curve with laboratory data on larval growth rates. The ELEFAN program uses time-series length-frequency data to project a growth curve backward in time to a hatching date. The agreement between the ELEFAN curve and larval growth data from IrmDA (1984) is striking (Fig. 4, Table 3). This suggests that the inefficient sampling of juvenile and larval krill by the 6 mm mesh trawl did not bias the population structure towards the larger size classes to the extent that the growth curve was unduly distorted.

Growth rates obtained from ELEFAN overlapped with existing values in the litera- ture. Maximum growth rates in the fast growth season were 0.125 mm day -1 for Group 0 krill, 0.082 mm day -1 for Group I and 0.041 mm day -1 for Group II. The maximum growth rates of Group I and Group II krill were lower than the summer growth rates of 0.105-0.179 mm day -1 estimated by ROSENaERC et al. (1986) from the Discovery expedition samples. Maximum growth rates of Group 0 krill were within the range estimates by ROSENBERG et al. (1986). Growth rates of all three age classes were less than maximum at low chlorophyll concentrations. These results indicate that both the age class and the food concentration should be considered when assessing the population growth of krill.

One of the main reasons for re-examining the growth rates of E. superba has been to determine the generation times of the species (egg to egg). This information is necessary when estimating sustainable catch rates in the developing krill fishery. Ir, EDA (1985) estimated krill generation times of 700, 760, or 820 days for animals growing for 4, 5 or 6 months of the year and attaining sexual maturity at a size of 35 mm. The ELEFAN program predicts that krill in Admiralty Bay would attain 35 mm size in 480 days. E. superba in Admiralty Bay appear, however, to reach sexual maturity at a larger size than 35 mm. From Sa~EPNIK'S (1982) data, mature females in January-March (spawning season) were 44.4 mm long. ELEFAN predicts that these females would have taken 715 days to reach sexual maturity.

During the first 100 days, krill growth in Admiralty Bay was maximal. According to laboratory rearing studies (Ir, EDA, 1984), E. superba passes through the stages Nauplius I to Furcilia IV in the first 100 days under favorable conditions. Using a hatching date of 28 February, maximal growth should have continued until about early to mid-June. Growth

Table 3. Comparison of larval growth rates of E. superba measured by 1KEDA (1984) with those predicted from ELEFAN growth curve based on length-frequency

data

IKEDA (1984) ELEFAN

0 0.57 8 0.70

13 0.78 20 0.91 30 1.72 30 0.85 44 2.90 53 4.26 63 5.38 60 4.82 75 6.65 86 8.24 91 8.03 99 8.82

112 9.60 127 10.66 121 10.51

Day Length (mm) Day Length (mm)

342 s. McCLATCH1E

rates for krill older than 100 days obtained from ELEFAN were lower than IKEDA'S (1985) maximum growth rates (Fig. 4). This is about 3 months after the February-March peak in phytoplankton abundance, when food concentrations were approaching their winter minimum (Fig. 9). Food-limited growth of late-stage krill larvae appeared to begin when water column pigment concentrations declined below 40 mg Chl a m -2.

The ELEFAN growth curve does not appear to fit the population modes well during the period May 1979 to December 1979. Krill population modes shift towards smaller sizes from March 1979 to September 1979 (Fig. 3). ETrERSHASK (1983) interpreted the reduction of mean krill size over the winter months as evidence that negative growth was occurring in Admiralty Bay during the winter. Data for Thysanoessa inermis from a northern Norwegian fiord also shows reduction of monthly mean krill length in the winter, suggesting body shrinkage (FALK-PETERSEN and HOPKINS, 1981).

The ELEFAN interpretation of STEPNIK'S (1982) data does not support the hypothesis of negative growth in winter in Admiralty Bay advanced by ETrERSrlANK (1983) based on the same data. Natural mortality increases with size, and recruitment of juveniles to the adult population in winter will combine with this to shift population modes towards smaller sizes in winter. According to this analysis it is unnecessary to invoke negative growth to explain the population structure in Admiralty Bay.

Growth of E. superba is maximal only for the months when water column phytoplank- ton concentration exceeds about 40-100 mg m -2 (depending on the age class of the krill). In Admiralty Bay this only occurred during the bimodal phytoplankton blooms in the 6 month period November-April. For the remaining 6 months of the year, growth of E. superba was still positive, but limited by food availability. Only during the mid-winter month of July did the water column phytoplankton concentration approach the threshold for zero growth for older krill. It seems unlikely that negative growth occurred in 1979, although if phytoplankton concentrations declined below about 17 mg Chl a m -2 negative growth would be expected. However, E. superba is able to exploit other food sources, and if zooplankton were abundant enough in patchy concentrations, krill might never show negative growth in this region. Admiralty Bay is an exceptional krill habitat in that food concentrations there are more favourable than in many other krill habitats which are covered by ice in the winter. The krill growth pattern in Admiralty Bay is probably more representative of northern regions such as South Georgia.

HOLM-HANSEN and HUNTLEY (1984) used theoretical arguments to examine food- limited growth of E. superba. Based on HUNTLEY and BOYD'S (1984) allometric equations, they derived an equation to estimate the maintenance concentration of food (Cm, ~tg C m1-1) required by E. superba to meet its minimum respiratory costs:

Cm = 0.111 W °155, (5)

where W is the krill dry weight in mg. Using this equation and assuming a carbon:chloro- phyll ratio of 60, the minimum pigment concentrations required for growth of different age classes of E. superba was predicted. These predictions are compared with the data from Admiralty Bay.

Maintenance food concentration was predicted using equation (5) for 15, 35 and 50 mm E. superba representing Group 0, Group I and Group II animals. Body lengths were converted to dry weight using IKEDA and DIXON'S (1982) regression (corrected) and wet weight:dry weight ratio. Corresponding dry weights for the three age classes were 2.34, 37.64 and 112.96 rag. Cm was predicted to be 2.11, 3.25 and 3.85 ~tg Chl a 1-1 for each

Food-limited growth of E. superba 343

age class, respectively. Values as high as these predicted maintenance food concen- trations were never recorded in Admiralty Bay, even during the mid-summer maximum (Fig. 10). HOLM-HA~SEN and HutCrLEV'S (1984) maintenance food concentration corres- ponds to the threshold for zero growth in Fig. 12, and Table 2 (p', equation 4). Threshold values (p') were 9.2, 12.5 and 17.5 lag Chl a m -2 for Group 0, Group I and Group II krill, respectively. Thresholds were expressed in terms of depth-integrated Chl a concentration (lag m -2) but can be related to volume concentration (lag 1-1) because concentrations approaching thresholds for zero growth only occurred during the winter when pigment concentration was vertically homogeneous (Figs 9 and 11). At this time (July) mean volume concentrations for both stations were between 0.06 and 0.1 lag Chl a 1-1 at different depths. These values are considerably lower than the maintenance concentrations predicted by HOLM-HANSEN and Hu~rLEV'S (1984) equation.

HOLM-HANSEN and HUNTLEV (1984) used an assumed balance between the terms of a simplified energy budget equation to derive their formula (equation 5). As Ross (1982) pointed out "one can reach erroneous conclusions if one uses measured physiological rates to predict a rate that is not m e a s u r e d . . . The predicted rate will include all the errors in the measured rates in addition to any omitted physiological functions". In their simplified budget Holm-Hansen and Huntley omitted the soluble excretion term, and have applied approximate values for assimilation efficiency and the respiratory quotient. A major source of error in their equation may have arisen from incorporating filtration rates of dubious quality cited in MORRIS (1984). Virtually all of these rates (MORRIS, 1984, his Table 1) are now known to be too low by a factor of 2-10 times (see BOYD et al., 1984; PRICE et al., in press).

Water column pigment concentrations fell below 0.1 lag Chl a 1-1 during July at Sta. 8 in Admiralty Bay, where the minimum integrated concentration was 16.6 ktg Chl a m -2. Mean values for both stations in Admiralty Bay during the mid-winter months of July- September were higher than threshold values, between 26.5 and 37.1 lag Chl a m -2, with the minimum in July.

Laboratory experiments demonstrated that growth rate of E. superba is proportional to food abundance up to 1000 lag Chl a 1-1 (IKEDA and THOMAS, in press), which is equivalent to 16.6 lag Chl a 1-1 using a carbon:chlorophyll ratio of 60 (HOLM-HANSEN and HUNTLEY, 1984). IKEDA and THOMAS (in press) found that juvenile krill fed Phaeodacty- lum tricornutum could just achieve positive growth at a food concentration of 0.33- 1.67 lag Chl a 1-1. These values are higher than the threshold concentrations estimated from the ELEFAN analysis (0.06--0.1 lag Chl a l-l), but the difference may simply be that the natural phytoplankton assemblage is more suitable food for krill than P. tricornutum. The krill used by IKEDA and THOMAS (in press) were 16-25 mm in length corresponding to immature Group I krill from Admiralty Bay. Maximum growth rates for Group I krill (0.04-01 mm day -1) overlapped with the laboratory growth rates (0.005--0.09 mm day -1) recorded by IKEDA and THOM_aS (in press) at high food concentrations.

The ELEFAN interpretation suggests that E. superba can meet their minimum main- tenance requirements at much lower concentrations than suggested by HOLM-HANSEN and HUNTLEY (1984). This is hardly surprising since the biomass of phytoplankton in the Southern Ocean is generally low (0.03-1 lag Chl a 1-1, EL SAVED and TURNER, 1978). Blooms of phytoplankton occur in the Southern Ocean (EL SAVED, 1971; FRYXELL et al., 1979; SMITH and NELSON, 1985) but they are spatially and temporally limited in extent. While it may be that krill must find high concentrations of patchily distributed food to

344 s. McCLATCHIE

grow, it is more likely that they possess the ability to survive (resist starvation) and grow slowly in their dilute environment but with the ability to exploit high density food patches when they occur.

Acknowledgements--I am grateful to M. Lipsld (Institute of Ecology, Dzlekanow Lesney, Poland) for permitting the use of his phytoplankton pigment data prior to publication. Helpful comments offered by T. Ikeda, J. M. Bradford, and D. Pauly significantly improved the manuscript. Support during manuscript preparation was provided by a New Zealand University Grants Committee Postdoctoral Fellowship at Portobello Marine Laboratory, University of Otago.

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