Mar 5, 1984 - roughly 8 to 9 days from field data (Brinton and Town- send 1984), 11 ... The volume of water sampled during a tow was in the range of 600 to ...
Polar Biol (1986) 5:221-234
© Springer-Verlag 1986
Larvae of Euphausia superba in the Scotia Sea and Bransfield Strait in March 1984 - Development and Abundance Compared with 1981 Larvae Edward Brinton, Mark Huntley and Annie W. Townsend Scripps Institution of Oceanography, A-001, La Jolla, CA 92093, USA Received 19 June 1985; accepted 14 November 1985
Summary. Larvae of Euphausia superba in the Atlantic sector of the Antarctic in March 1984 averaged 580 per 1000 m 3 of water. This is 100 times less than we observed in March 1981, but more than the average of 250 larvae per 1000m a found in January-February 1981. There was one 1984 high-abundance sample, accounting for 85% of all larvae caught, from the eastern area of confluence of Drake Passage and Weddell Sea waters. Abundances in 1984 near the South Shetland Islands were commonly 5 to 10 larvae per 1000 m a, and younger by 2 to 4 developmental stages than in March 1981. Body lengths of given stages were generally less in 1984 than in 1981. Advanced furcilia stages, particularly, in the 1984 samples tended to be smaller than the same stages in March 1981, indicating relatively poor growth during February 1984. However, the 1984 younger larvae (calyptopes and the developmental forms of furcilia stages I and 2) indicated that, in 1984, recent (March) growth had been good - probably better than in February. Direct observation of the development of calyptopis stage 3 to furcilia stage yielded a development time of 7.7 days, which compares favorably to the 8-day period estimated from field samples. Reduced food availability did not affect the development rate nor give rise to a clearly higher incidence of indirect pathways of development. It is postulated that recruitment was about of month later in 1984 than in 1981 in most of the area studied and was probably going to be less successful. Introduction In spite of the vaunted ecological importance of Euphausia superba in waters surrounding the Antarctic continent, this species remains incompletely understood in many respects, such as recruitment rate, duration of life phases and, particularly, abundance in space and time. Attention, here, will be given to distribution, abundance, and developmental condition of larvae collected during March 5 to 26, 1984, with comparisons being drawn with
results of similar sampling during January to March, 1981. Data exist on spatial and seasonal relationships of aggregations of adult krill to concentrations of larvae (e.g. Marr 1962; Makarov 1972; Brinton and Townsend 1984), resulting in attempts to interrelate occurrences of the different developmental states and determine environmental dynamics responsible for population maintenance (Mackintosh 1972; Brinton 1985). However, we still do not know, for example, whether eggs and larvae found in the Bellingshausen Sea, Bransfield Strait, Scotia Sea, or Weddell Sea derive from local production and persist through local processes, or whether infusion and diffusion of larvae and juveniles predominate. The complex and inconsistent hydrography of these regions of confluence of water types (e.g. Foster and Middleton 1984; Stein and Rakusa-Suszczewski 1984), particularly near the South Shetland Islands, hampers attempts to generalize about life cycles, including success of annual production, timing of life phases, and age structure and reproductive capacity of the parental stock. Marr's (1962) description showed that January to March are most important for reproduction in E. superba. The resurgence of studies of krill in the Atlantic sector of the Antarctic, since industrial interests began in the mid-1960s, provides new evidence of yearto-year differences in the amount and timing of reproduction (Table 1). Data are not available for all years 1965 to 1983. This evidence indicates that reproduction was likely to have been successful in 8 of the 11 seasons documented. 1967, 1978, and 1983 were probably poor years. The early life history of E. superba has also received much recent attention. (1) Spawning probably takes place above 250 m (George 1984), based on experiments with effects of pressure. (2) Embryonic development occurs while the eggs sink and takes 3 to 4 days (McWhinnie and Denys 1978) or 5 to 6 days (Ross and Quetin 1982). (3) Nauplii hatch at about 850 m (Quetin
222 Table 1. Published information on krill reproduction during 1965 to 1983, Scotia Sea, Bransfield Strait, and Antarctic Peninsula waters Year
Months
Place
State of larvae
1965 1967
Jan. to early Feb. Feb.
Abundant calyptopes No larvae
1967
March
Scotia Sea N, E, and SE of Elephant I. Scotia Sea
1969
Jan. to early Feb.
Scotia Sea
1969
Late Feb. to mid-March
Scotia Sea
1976
Scotia Sea, westward
1976
Mid-Nov. (1975) to midJan. (1976) Late Jan.
Early calyptopis and early furcilia stages widespread and predominant Late calyptopis and early furcilia stages widespread and predominant Gravid females and larvae Calyptopes widespread and numerous
1976 1976
Early Feb. Late Jan. to early Feb.
1977
Jan. to mid-March
Near Elephant I. Near Anvers and King George Is. Scotia Sea, westward
1977 1978 1978
Jan. Early Jan. Jan. to Feb.
SE Weddell Sea Scotia Sea Bransfield Strait
1978
Nov. (1977) through March (1978)
Scotia Sea
1978
Nov. (1977)through March (1978)
Near South Georgia
1979
Jan. to Feb.
Scotia Sea
Larvae present
1979
Mid-Jan. to mid-Feb.
Female krill with eggs
1980
Jan. to Feb.
Admiralty Bay (South Shetlands) Admiralty Bay (South Shetland)
1981
Late Jan. to mid-Feb.
Scotia Sea, from 50°W eastward
1981
4 to 23 March
Scotia Sea, from 46°W westward, Elephant I., Bransfield Strait
1981
19 Jan. to 19March
Scotia Sea, from 42°W westward, Drake Passage, Bransfield Strait
Abundant calyptopes, C 1 dominant, very few furciliae Abundant furciliae, calyptopes continuing to be produced, but fewer than in Jan. to Feb. Abundant calyptopes throughout Feb., lacking by mid-March. Furcilia maximum in late Feb.
1981
Feb. to March
Bransfield Strait and N side of South Shetlands
Bransfield Strait eastward to N of South Orkneys
Larvae retarded in development compared with 1965
Calyptopes numerous Many large gravid females Gravid females and larvae Abundant calyptopes No eggs or larvae Peak spawn in first half of Feb. No larvae before Jan. Few during Jan. to Feb. Highest abundances (calyptopes) in March, particularly near Antarctic peninsula, South Shetlands Larvae present, particularly in March
Female krill with eggs
Larvae abundant
Author's comment
Author Makarov 1974 Makarov 1974
"Thermal conditions" of a particular year may control emergence of calyptopes 1969 more like 1965 than 1967
Makarov 1974
Makarov 1974
Makarov 1974
A particularly early breeding Hempel (1985a) regards 1976 larvae to be in "fair numbers" in Bransfield Strait, northern Scotia Sea
Intense breeding through period
Late spawning
Witek et al. 1980 Hempel and Hempel 1978
Nast 1979 Jazdzewski et al. 1978 Witek et al. 1980 Fevolden 1980 Witek et al. 1980 Hempel et al. 1979
Thysanoessa was strongly dominant larval euphausiid
Hempel 1981
Larvae more numerous than in 1976, 1977, but fewer adults More Jan. to Feb. reproduction than in 1978 More numerous than in 1978 Maximum numbers in early Jan., - earlier, even, than 1979
Hempel 1981
Witek et al. 1980
Rakusa-Susczewski and Stepnick 1980 Jackowska 1980
Brinton and Townsend 1984 Indicates significant breeding from early Jan. into late Feb.
Brinton and Townsend 1984
Spawning could have begun by early Dec., most intense late Dec. to early Jan., ending Feb. in Bransfield Strait, somewhat later toward east
Rakusa-Susczewski 1984
Kittel and Jazdzewski 1982
223 Table 1 (continued)
Year
Months
Place
State of larvae
Author's comment
Author
1981
Jan. to March
Central Scotia Sea, Elephant I., Bransfield Strait
Late Dec. (1981) to early March (1982)
1982
30 Jan. to 3 March
Smith I., South Shetlands, Gerlache Strait/Melchior Sound (W of Antarctic Peninsula), N and S of Elephant I. Scotia Sea, South Orkneys, Elephant I., Bransfield Strait, Antarctic Sound
Larvae significantly more than in 1976, 1978; larvae rare in N o v . - Dec. 1981 Schools of gravid females throughout study period, S of Elephant I., W of South Shetlands, and near Smith I.
Hempel 1985a
1982
Larvae abundant, particularly in central Scotia Sea and shelf region near Elephant I. (Does not deal with larval abundance)
1983
Late Jan. to early Feb.
Admiralty Bay (South Shetlands), Bransfield Strait, Palmer Archipelago, Gerlache Strait/Charlotte Bay (W of Antarctic Peninsula)
Larvae mainly calyptopes, few furciliae, throughout area, moderate numbers compared with 1981, eggs widespread (Does not deal with larval abundance)
and Ross 1984b) or 1000 to 1200m (Marschall and Hirche 1984), estimated using experimentally determined sinking rates (variable even within a brood according to George and StrOmberg 1985) and length of embryonic life. Field data show that some eggs and nauplii occur still deeper (Marschall and Mizdalski 1985; Hempel 1985b). (4) The metanauplius stage is reached during active "developmental ascent" (Marr 1962), 13 days (Marschall and Hirche 1984) or 15 to 18 days (Ross and Quetin 1982) after spawning; yolk absorption continues until calyptopis stage 1 is attained (the first feeding stage, Marschall 1984) in the euphoric zone, after 21 to 25 days (Ross and Quetin 1982) or 30 days (Kikuno 1981) of development. (5) The duration of the three calyptopis and six furcilia stages may vary among stages and conditions roughly 8 to 9 days from field data (Brinton and Townsend 1984), 11 to 12 days for calyptopis 1 in the laboratory (Ross and Quetin 1982), and 9 to 15 days per stage, also in the laboratory, on a defined diet (Ikeda 1984). Still longer stage durations were estimated from field data (Witek et al. 1980). Using any of these rates, larval life will extend from midsummer (January-February) until April at the earliest; there are a few late furcilia specimens showing it may extend to December (Marr 1962). In this paper we apply a new method, developed for copepods by Miller et al. (1984), which permits direct observation of the development rate of field-collected larvae. (6) In November to early December 1983 in the southern Scotia Sea, most overwintered adolescents caught were 15 to 25 mm (range, 11 to 31 mm) (Brinton 1984), including one larva of furcilia 6. (This compares favorably with growth to 20 to 25 mm in the laboratory, also
Quetin and Ross 1984a
Marschall and Mizdalski 1985
Reproductive krill (>45 ram) few, females with spermatophores rare, indicating "limited spawning"
Fevolden and George 1984
over 9 months, Marschall 1984). (7) Larger krill, most believed to be a year older, were then 40 to 54 mm, but not yet spawning. Finally, in summer (December to March) the stocks become reproductive, sometimes still showing clearly bimodal body-length distributions, e.g. in 1981 (Brinton and Antezana 1984) and in 1982 (Quetin and Ross 1984a). When such bimodal structure is indistinct, the merging of modes representing year classes may be a consequence of mixing of populations having regional or temporal differences in (1) growth rates of the young krill and (2) duration and timing of recruitment (Brinton and Townsend 1984), or growth rates of older krill, e.g., differences in winter among feeding vs. starved krill (with even the possibility of body shrinkage, Ikeda and Dixon 1982) and in summer among reproductive vs. nonreproductive krill. Evidence as to similarities and differences between 1983 - 1984 and other years, particularly 1980- 1981, considering, now, the 1984 larvae, are the subject of this paper.
Methods FieM Observations Larvae of Euphausia superba were collected by R VMelville on Protea expedition (Leg 6) (Fig. 1) using paired bongo nets having mouth widths of 0.71 m and mesh widths of 0.333 mm. Nets were towed obliquely at 2 to 3 knots, usually 0 - 2 1 0 - 0 m in open waters of the Scotia Sea and 0 - 1 4 0 - 0 m near islands and the Antarctic peninsula. These depths are not expected to be deep enough to catch all of the still upward-migrating calyptopis 1 (Hempel 1985b; Marschall and Midzalski 1985). The volume of water sampled during a tow was in the range of 600 to 1000 m ~, and the towing distance, 0.5 to 1.5 km.
224 Most samples were sorted for larvae in their entirety because abundances were generally low. When the larvae were numerous, they were subsampled with a Folsom plankton splitter. Larvae in good condition were selected for measurement of body length, tip of rostrum to tip of telson. We follow Fraser's (1936) definitions of the stages in E. superba: the calyptopis phase (3 stages) includes postnaupliar larvae without pleopods and with eyes covered by the carapace; furcilia stage I includes all forms of furcilia without setose pleopods (0 pleopods, 1 to 5 nonsetose pleopods = 1' to 5'); furcilia stage 2 includes all forms with a combination of nonsetose and setose pleopods, plus the form combining 5 setose pleopods (5"), 7 terminal telson spines and 3 pairs of unaltered posterolateral telson spines. Furcilia 3, having 5 pairs of setose pleopods (5"), is distinguished by the number and form of telson spines, shape of rostrum, and number of photophores. The number of telson spines is used to recognize stages 4 to 6. Because of the sparse occurrences of larvae in 1984 compared with 1981, statistical testing of differences between the periods and regions was generally limited to simple comparisons of curves illustrating developmental stage vs abundance. Abundances of stages have been averaged, regionally, even though larvae at a given station may include stages not present at nearby stations - again, because of the frequently low abundances of larvae.
Direct Observations of Development Development rates of Euphausia superba calyptopis larvae were determined using a modification of the "molt-frequency" technique intro-
60ow
55 °
54°S
duced by Miller et al. (1984). Given the rarity of larval krill in 1984, we were able to conduct but a single experiment, in which we observed the development to furcilia stage 1 from calyptopis stage 3. Live zooplankton were collected in a 0 - 50 m vertical tow of a 1-m net, equipped with a 15-1 protected cod end (Reeve 1981), at station 2 in the mid-Scotia Sea (58°S, 39°W; see Fig. 1). Live calyptopis stage 3 larvae were sorted into seven lots of approximately 50 each, and each lot was placed into separate 1-1 containers of filtered seawater until the sorting procedure was completed. More than 2001 of water were collected for the experiment from a depth of 30 rn, using a centrifugal pump. The water was placed in a 200-1 Nalgene tub until larval stages had been sorted (approximately 2 h). To begin the experiment, each lot of 50 larvae was transferred to separate 10-1 carboys filled with thoroughly mixed seawater from the 200-1 tub. The carboys were then sealed and p!aced on a l-rpm grazing wheel (Huntley et al. 1983). The entire experiment, including the sorting of larvae, was conducted in a refrigerated van at a controlled temperature of + 1.0°C. Over the following five days (127 h) carboys were removed from the wheel, one at a time, at approximately 24-h intervals. After each carboy was removed, the larvae were screened using coarse Nitex mesh and preserved in 10°70 formalin. Triplicate 500-ml samples of water were taken for immediate chlorophyll analysis (Strickland and Parsons 1972). Preserved larvae were then examined microscopically, within several hours, to determine (a) how many had molted to the next stage, furcilia 1, (b) whether their pleopod morphology indicated direct or indirect development, and (c) the fullness of the gut. Gut contents were estimated by eye as either 100, 75, 50, 25 or 0°70 full. Development rate
50 °
45 °
,
,
40 °
, sou,L,:, 4 .2 v. 5 4 ° S
PROTEA EXPEDITION., LEG 6
March 5-27, 1984
C a l y p t o p i s Larvae and 56 °
ORDER IN WHICH STATIONS WERE OCCUPIED
56 °
®
q~
58 ° --
I
SCOTIA SEA
% 90- I00
58 °
eo
2.
4 50
DRAKE PASSAGE
089
600 A
60 ° -
58,59, J _78_85 88° IJA,. II# Elephant I
-
60 °
(~5 No. per I O 0 0 m 3
E,,
~\e'
~ 8 5 O] o - " ~ ' ~
~,o~
"~
South Orkney Is.
~-':~'~
• 1-25
......
62 °
o Zero
@ 2 6 - 250 •
62 °
251 - 2 5 0 0
(~) 2501 - 2 5 , 0 0 0 1>25,000 64 °
,.-e~~'.'.',,.-~l ~" (e vq
i
I
I
I
64 °
40 ° 55 ° 50 ° 45 ° Fig. 1. Abundances of calyptopis larvae ofEuphausia superba at localities sampled by bongo nets in the sequence indicated, during March, 1984, in the Scotia Sea and Bransfield Strait. Area A (small square north of Elephant Island) includes stations 27 to 57, 60 to 77, 86 and 87. (In Figs. 4, 6 and 60°W
7, Protea expedition stations are given the prefix "P", e.g. P-l, to distinguish them from Vulcan expedition (1981) stations)
225
Furciliae were fewer than 25/1000 m 3 at 26 of the 27 positive stations (Fig. 2). The highest abundance, 948 per 1000 m 3, was from the same station in the mid-Scotia Sea at which calyptopes were most abundant. The predominance of calyptopis stages 1 and 2 (Ci, C2) during March 5 to 8 in the Scotia Sea east of 50°W is evident in five of the six stage-frequency distributions (Fig. 3). We noted in "Methods" that C1 is underestimated due to depth of sampling. At Protea expedition station 3 (P-3), nearest the South Orkneys, C2 was dominant, but C3 outnumbered C1. In this area, furciliae occurred only at station 2, and 86°7o (818/1000 m 3) were stage 1 (F0. To the north of Elephant Island during March 16 to 25, 59 plankton samples obtained within 20 km of the northern side of the island (area "A" and 7 adjacent stations, Figs. 1 and 2) yielded an average of only 2.9 larvae per 1000 m 3 (1.7 calyptopes and 1.2 furciliae) (Fig. 4A), the range being 1 to 21/1000 m 3. The stage-frequency curve peaked at C2 and at F 3. Thirty-five of the 59 samples were negative for larvae.
was determined by plotting against time the percentage of larvae molted at each successive time interval.
Results
Regional Differences in Abundance Larvae of Euphausia superba were present in 42 of the 100 samples obtained during March 5 to 27, 1984. Calyptopis larvae outnumbered furcilia larvae in all areas sampled (Figs. 1 and 2), dominating overall by 48:1. Eighty-five percent of all larvae caught were from one station in the mid-Scotia Sea, 58°S, 39°W, halfway between South Georgia and the South Orkney Islands (Fig. 1), where there were 41,000 larvae per 1000 m 3, to 210 m depth. We did not sample further until near the South Orkneys. Substantial numbers (>250/1000 m 3) were caught at only four additional stations, three of which were northwest of the South Orkneys and one in the Bransfield Strait. At 33 of the 42 positive stations there were fewer than 25 calyptopis larvae per 1000 m 3.
60ow
55 °
50 °
45 °
40 °
I
I
I
I
I
54°S
S o u:'t h " G ~ " " -
54°S
PROTEA EXPEDITION., LEG 6
o~'~~
No. per I O 0 0 m 3 - - 6 2 ° o Zero
~ "
.
~.--~
"'i
• 1-25
(none) 2 6 - 2 5 0
WEDDELL SEA o
•
. -~,'i~'
I
I 60°W
55 °
Fig. 2. Abundances of furcilia larvae of E. superba
50 °
251 - 2 5 0 0
45 °
40 °
-
-
64 °
226
-
__
1o422"
id ~E O O O
imens of older furcilia stages (F 3 to Fs) were caught in this westernmost part of the study area, all within the Bransfield Strait. The stage-frequency curve from the Strait showed modes at C2 and at F 2 (Fig. 4C). The shift in dual modes of C2 to F 3 at Elephant Island to C2 and F 2 at King George Island may have been because the former sampling was 5 to 10 days later than in the Bransfield Strait.
ABUNDANCESOF LARVAE SCOTIASEA, MARCH5-8,1984
~TAI/X/\
\
P-4 P-5 P-I
1984 Abundances Compared with 1981
IO!
Qr~ hl rn
Stations P-1 and P-2 (1984) were located in the same part of the mid-Scotia Sea (Fig. 1) as were Vulcan expedition (1981) stations V-62 to V-72 which were separated by increments of 10 km (Brinton and Townsend 1984). The 1984 stations were occupied on March 5 and the 1981 stations during February 3 to 4. Station P-1 yielded a curve for abundance vs. developmental stage (Ct, C2) much like station V-64 (Fig. 5), and station V-72 showed the same developmental stage composition, though abundance was 100 times greater. Station P-2 (1984), on the other hand, resembled stations V-62 and V-66 (1981) with respect to both abundance and the broader spectrum of stages. Farther to the west, northeast of the South Orkneys, we were able to compare March 1984 larvae with March 1981 larvae. The 1984 stations P-4 to P-6 (Fig. 1) were positioned to correspond with the 1981 stations V-159A1, V-159A-2, and V-160-1 (Brinton and Townsend 1984) in the region where 1981 larvae had been most abundant, ca. 4 x 105/1000 m 3. However, 1984 larvae, here, were fewer than 103/1000 m s at all three stations, P-4 to P-6, and only calyptopes were present (Fig. 6A). Pursuing a possibility that most recruitment in this westerly area was to be a month later in 1984 in 1981, a
P-3
Z
,o !
CI
C2
C5
El
F2
F3
F4
F5
CALYPTOPIS FURCI LIA Fig. 3. Abundances of larvae of E. superba, by developmental stage at Protea expedition stations 1 to 6
To the south of Elephant Island on March 10, calyptopes (Ct to Ca) were present, at a density of 69 larvae per 1000 m s (Fig. 4B). Fourteen days later (March 24), C2, C3 and a few of FI were found there, at 44 larvae per 1000 m3; this suggests a longer stage duration than the 8 days inferred above, unless March 10 was shortly after a general advance in stage and March 24, shortly before one. Near the South Shetland Islands during March 11 to 15, larvae were found to the north of King George Island and in the Bransfield Strait (Fig. 4C). A total of ten spec-
102
A
.
B
II II
,X OF 59 Stas. in and near Area A, North side Elephant I. March 16-25
fS
(I-- --r-e
of Elephant T. (Sta. 7) March I0
~'~-~
IO
I
S ond W
\ i
of Elephant I. (Stas. 84, 85)
/
\~ \\
~,
Bransfield Strait (,X of 5 stas.)
March13-15
//~/'/*(~'q\\\\
% 0 0 0
/I l I
c
-Z
n-I W 12. n~ W rn
\
N 0_f King George T.\ z oJ
.01
I
C2 C3 CALYPTOPIS
Cl
Fl
F2
F3 F4 FURCI LIA
F5
Fs
CI
C2
C3
CALYPTOPIS
FI
FZ
F3
FURCILIA
F4
\
(~ of 3 stae.)
--.\
Marchll- 12
\
CI
P C2
I C3
CALYPTOPIS
I Fj
\ \ \
\
\
\ I
\
\
~ F2
I F3
I F4
FURCIUA
Fig. 4 A - C. Mean abundances of larvae of E. superba, by stage A north of Elephant Island; B south and west of Elephant Island, sampled with 14day interval; and C in the two most westerly regions sampled
227 ABUNDANCES OF LARVAE, BY DEVELOPMENTAL STAGE, IN AREA 56°-58°S, 59°W OF SCOTIA SEA
comparison was made between late January 1981 data (stations V-2 to V-12) and early March 1984 data (stations P-4 to P-6) f r o m the same place. Figure 6B Shows stage-composition to be essentially the same in both sets of data, but abundances were generally 10 to 20 times greater in 1981.
Spatial and Temporal Differences in Body Length, by Stage
%
O n~ bJ 12n~ W
Z I0
Cl C2 C3 Fi F2 F3 F4 F5 CALYPTOPIS FURCILIA Fig. 5. Abundances of larvae of E. superba, by stage, comparing March 1984 data, heavy lines (Protea expedition stations P-I, P-2), with February 1981 data, thin lines (Vulcan expedition stations V-62 to V-72), from some area
In order to use means other than abundance to assess suitability of the different environments for survivorship and recruitment, consideration will be given to bodylength of individual developmental stages, by region (Table 2). Larvae f r o m the open Scotia Sea (stations P - l , P-2) yielded a length-stage curve (Fig. 7) in which body-length was average through F 1 but above average in F2 and F3 (P < 0.01 for F2 and F3, Rank Sum test). The one F4 larva was small. Figure 8 shows that this curve (open Scotia Sea, March 5, 1984) was particularly like that f r o m the same region during January 24 to February 14, 1981; in both, the more advanced furcilia stages seem to fall progressively nearer to the smallest regional values - f r o m north and northwest to the South Orkneys, March 16 - 18, 1981. This trend in direction of the curve was interpreted (Brinton and Townsend 1984) as showing good growth in the recently emerged calyptopis stages and that there had been poor growth a m o n t h or so earlier when the "present" (March 1981) furciliae were in the calyptopis phase. This interpretation is supported by the ex-
A B U N D A N C E S OF L A R V A E N O R T H OF S O U T H O R K N E Y ISLANDS 1984 (Heovy lines)vs 1981 (Light lines) MARCH 18, 19, 1981 vs MARCH 8, 1984
JAN. 24, 25, 1981 vs MARCH 8, 1984
I06
I05
oO,OV// L V 59A-IF /
/
_
&
I '98'1/Vl'°A-2
\
\
/
/
P
J12
~i.~1~v4
\
7,0
ill S
ill
~
-P5
I02 -VI# IO
Ci
C2
Ca
CALYPTOPIS
FI
F2
F3
F4
FURCILIA
F5
F6
P
Ci
C2
C3
CALYPTOPIS
F~
I
F2
I
F3
FURCILIA
Fig. 6A, B. Abundances of larvae of E. superba, from same area north of South Orkneys, comparing 1981, thin lines (Vulcan expedition stations, with prefix V) and 1984, heavy lines (Protea expedition stations, with prefix P). A March 1981 and March 1984; B January 1981 and March 1984
228
Table 2. Mean length (in mm) and standard deviation of calyptopes and furciliae of Euphausia superba in areas sampled, 5 - 2 4 March 1984 Area sampled
Calyptopes
Open Scotia Sea (5 March) Near South Orkneys (North Side) (7 March) NW of South Orkneys (8 March)
North of Elephant I. ( 1 6 - 2 5 March) S and SW of Elephant I. (10 March)
C1
C2
C3
F1
F2
F3
F4
F5
1.97 (-+ 0.10) 1.89 (1 only) 1.96 (_+0.14) -
2.99 (_+0.35) 2.97 (_+0.18) 2.67 (_+0.19) 3.08 (_+0.23) 3.08 (_+0.32) 3.20 (_+0.11) 3.21 (_+0.12) 3.35 (_+0.16)
4.35 (_+0.40) 4.27 (+0.12) 3.66 (_+0.23) 4.32 (_+0.36) 4.61 (_+0.02) 4.46 (_+0.18) 4.49 (_+0.57) 4.21 (_+0.35)
5.42 (_+0.48) . .
6.80 (+0.29) .
7.78 (_+0.27) . .
7.64 (1 only)
-
8.05 (_+0.34)
9.09 (_+0.06)
7.75 (_+0.18)
9.30 (1 only)
2.02 (_+0.11) 2.02 (_+0.12) 2.02 (_+0.11) 2.02 (_+0.09)
South of Elephant I. (24 March) North of King George I. (11 - 12 March) Bransfield Strait (13 - 15 March)
Furciliae
tremely small numbers of older furcilia larvae in both January-February 1981 and March 1984. That is, abundance (as well as body size) of these furciliae reflects earlier environmental conditions which influenced (1) their initial production and/or (2) subsequent mortality. Further, it seems unlikely that good growth in calyptopes would be simultaneous with poor growth in furciliae. Other 1984 data (Bransfield Strait, north of Elephant Island, Fig. 7; south and west of Elephant Island, Table 2) are also aligned with the "open Scotia Sea" data for 1984. This could indicate that, prior to our times of sampiing, growth had been poor through much of the study area. Northwest of the South Orkneys (stations 4 to 6, Fig. 1), body lengths of C 2 and C 3 w e r e small compared with calyptopes elsewhere (Fig. 7). Older larvae (Ca, FI) oc-
.
E E
N.ofElephant I. .../ /"
Ip(D Z Ld
Open Scotia S e e ~
Ix 6
.
5.50 (_+0.64) . .
6.39 (_+0.56) .
7.37 (_+0.48) . .
5.23 (_+0.24) 5.98 (1 only) 5.33 (_+0.26)
.
.
.
.
.
.
.
.
6.35 (_+0.62)
7.11 (_+0.41)
So.of Elephont I. 10,1.5March 1 9 8 1 ~ No.of Elephont I. Morch 20- 2 3 , 1 9 8 1 ~
~ "----.~/// //
//
/ /
/ /) ~ . f - - //47 -
8
/
/
~,~¢~P"4 /o~",~a
/ /
~6 g
N.of Ki
.
S I Z E S OF L A R V A E FROM OPEN SCOTIA SEA AND ADJACENT REGIONS, 1984 AND 1981
E I'(-9 zS--
.
curring north of King George Island averaged somewhat larger than larvae of the same stages in the other regions (except for C3, south and southwest of Elephant Island, March 10, Table 2); however, C2 larvae - the most abundant stage - averaged insignificantly smaller north of King George Island than in the Bransfield Strait; C2 larvae from the Bransfield were also more numerous than north of King George Island (Fig. 4C). Larvae from north of Elephant Island and from the Bransfield Strait were not only similar in stage-frequency structure (Figs. 4A, C), but also the most similar in body length, stage-by-stage (Fig. 7).
SIZES OF LARVAL STAGES, BY REGION MARCH 5 - 2 4 , 1984 Bransfield~--S, ~
.
ope. soo.o Seo
/ ~ N and NW of So.Orkneys March 16-18,1981
IX
4 ~ " ~N~(of SouthOrkneys
f/~-/~w
ofSo.Or,°eys
//.6"¢/f
,L:~-/ Cl
- C2
//I
C3
CALYPTOPIS
I Fi
I F2
I F3
I F4
2 F5
FURCI L IA
]Fig. 7. M e a n body lengths o f larvae o f E.
c~
c2
I
c3
CALYPTOPIS
superb°, by stage,
March
1984, from all stations in each of five areas investigated. Open circle indicates single specimen. Values and standard deviations are given in Table 2
I
F,
I
F2
I
F3
I
F4
~
F~
I
F6
FU RClLIA
Fig. 8. Mean body lengths of larvae of E. superba, by stage, comparing 1981 (data from Brinton and Townsend 1984) with 1984. Open circle indicates single specimen
229
A comparison is made in Fig. 9 between 1981 and 1984 average sizes of larval stages from three of the regions not compared in this way in Fig. 8: (A) to the north of Elephant Island, (B) to the south and southwest of Elephant Island, and (C) the Bransfleld Strait. In the three places the younger larvae are similar between the two years, while older stages show progressively increasing differences, with 1984 furciliae averaging smaller by more than 1 mm in stages F 3 and F 4.
Variation & Developmental Pathway As discussed in detail in Fraser (1936); Makarov and Maslennikov (1981), and Brinton and Townsend (1984), larval development during furcilia stages 1 and 2 includes the addition and, finally, fully setose development of the five abdominal pleopods. This may be accomplished in two or more molts, with different sequences being different "pathways" of development. In the most direct pathway, calyptopis 3 develops into a furcilia 1 having five non-setose pleopods (form 5' of furcilia stage 1) which, in turn, develops into a furcilia having five setose pleopods (form 5" of furcilia stage 2). The second most direct pathway through furcilia stages 1 and 2 is considered to be 4 ' ~ 4 " 1 ' ~ 5". Both of the above pathways are believed to reflect rapid development in response to favorable field environment, as has been observed in the related species, E. pacifica (Knight 1984). Other pathways seem to reflect slower development, for example, 3 ' ~ 3 " 1 ' ~ 4 " 1 ' ~ 5", under circumstances of unfavorable environment. Furcilia stages 1 and 2 were numerous only at station 2 in the mid-Scotia Sea (Fig. 3). Elsewhere, only a few specimens of those stages occurred, among the dominant calyptopes. At station 2, most (75%) of furcilia 1 were form 5', indicating good environmental conditions, and 17% were 4'. Of furcilia 2, most (59%) were 4"1' (developed from furcilia 1 having only 4', when environment was somewhat poorer), and 37% were 5". In the Bransfield Strait, the few furcilia stage 1 were with 3' or 4' pleopods. However, of furcilia stage 2, 60% were with 5", the remainder being 4" and 3"2'. To the north of Elephant Island, 7 of 10 specimens of furcilia 1 were form 5', 2 were 4', and 1 was 0'. 13 of 15 specimens
of furcilia 2 were form 5" and 2 were 4"1". Thus, direct, or relatively direct pathways were being followed by most of these larvae in March 1984.
Relationships with Chlorophyll In the 1981 data we looked for relationships between field concentrations of chlorophyll a and body sizes of the associated larvae (Brinton and Townsend 1984). Largest larvae, stage by stage, were found to be from water with the highest March chlorophyll value, south of Elephant Island. Smallest larvae (also the densest aggregations) were from water with the least March chlorophyll, northwest of the South Orkneys. None of the other (intermediate) chlorophyll values and sizes of larvae were correlated. Integrated water-column chlorophyll values were used in 1981. In 1984, only a few water-column measurements were made, while there were numerous surface measurements (data from T. Antezana and K. Ray). However, in these waters the relationship of surface chlorophyll to water-column chlorophyll seems to be sufficiently constant that surface values can be used to compare localities. In 1981, surface values averaged 1.05% (+ 0.42%) of water-column values (N = 85) and, in 1984, 1.19% (+_0.26%) (N = 7). We noted (Fig. 7) that there was little difference among the regions studied in March 1984 with respect to body sizes of larvae. This had not been the case in 1981 when average body lengths of given stages differed by as much as 50% between regions (Fig. 8). Sizes of 1984 larvae tended to be intermediate between the regional extremes of 1981 (Figs. 7 and 8). Similarly, 1984 chlorophyll values from all regions were intermediate between the extremes of 1981 (Table 3). In the open Scotia Sea (57-58°S, 38-39°W) Janua r y - February 1981 was similar to March 1984, with respect to body size and stage composition of larvae (Fig. 8) and surface chlorophyll. High chlorophyll values were obtained during both 1981 and 1984 from the north coast of the South Orkneys - both times in association with few krill larvae. Two hundred km northwest of the South Orkneys in an extensive swarm of larvae, March 1 6 - 18, 1981, chlo-
Table 3. Surface chlorophyll a (Ixg/1), 1981 and 1984 (1981 data from O. Holm-Hansen, 1984 from T. Antezana and K. Ray) Area sampled
1981 (Vulcan Expedition)
1984 (Protea Expedition)
Open Scotia Sea, 57 - 58°S, 38 - 39°W Near South Orkneys (north side) NW of South Orkneys, 59°S, 50°W
0.40 6.25 2.19 0.11 1.02 0.71 2.82 0.48
0.73 (_+0.38) (5 March) 2.80 (7 March) 0.34 (_+0.04) (8 March)
All Scotia Sea Stas, 3 4 - 5 0 ° W N of Elephant I. S and SW of Elephant I. Bransfield Strait N of King George I. Drake Passage (near 58°S, 60°W)
(+0.11) ( 3 - 4 Feb.) (+2.22) (27 Jan.) (+0.94) (25 Jan.) (17 March) (g for 24 Jan. to 14 Feb.) (_+0.26) ( 3 - 8 March) (10 March) (10 March)
0.37 0.42 1.18 0.37 0.19
( _+0.26) (_+0.08) ( _+0.77) (_+ 0.06) ( _+0.05)
(17 - 22 March) (11, 26 March) (13 - 15 March) ( 1 1 - 1 2 March) (26 - 27 March)
230 12 -A
NORTH OF ELEPHANT ISLAND
SOUTH AND SOUTHWEST
-C
,o
OF ELEPHANT ISLAND Morc~2iO- 23 ~ " ~ ~10 E vE T
./~
_
/i I/oro
BRANSFIELD STRAIT
Morch10,198
j/
(..9 zB-bJ I >E3 O 00 tX 6
/
.-{ ~ I~er!h '0, 24 /,~-,~8~,' 4--
J
// /S
2
i I Cl C2 C3 CALYPTOPIS
FI
i F2
I i F3 F4 FURCILIA
I F5
i F6
j' "
//
i i C2 C3 CALYPTOPIS
i Fi
i F2
I I F3 F4 FURCILIA
i
_(
F5
CI
I
i
i
i
I
i
I
C2
C3
FI
F2
F3
F4
F5
CALYPTOPIS
FURCIL IA
Fig. 9 A - C. M e a n body lengths of larvae o f E . superba, by stage, comparing 1984 with 1981. A north o f Elephant Island; B south and southwest of Elephant Island; C Bransfield Strait. Vertical bars show standard deviations
rophyll measured only 0.11 Ixg/1. In the same place, March 8, 1984, there were few larvae (Fig. 6), but chlorophyll was again at its lowest observed level (0.34 Ixg/1) except for measurements at the Antarctic Convergence, far to the northwest, in Drake Passage (Table 3). In the much studied region north of Elephant Island, chlorophyll was significantly less in 1984 than in 1981, 0.37 (+0.26) Ixg/1 compared with 0.71 (+0.26), while 1984 larvae were smaller as well (Fig. 9A). Southwest of Elephant Island in 1981 (March 10), chlorophyll measured 2.82 Ixg/1; three 1984 measurements (March 11, 26) averaged 0.42 Ixg/1. The 1981 larvae included C2 to Fs, peaking at Fi, and were larger, stage for stage, than in the other regions studied. The few 1984 larvae included only Ct to F1, peaking at C2-C3 (Fig. 4B), and, again, were smaller than in 1981 (Fig. 9B). In the Bransfield Strait, chlorophyll was insignificantly higher in March 1984 than in March 1981, while the 1984 larvae were fewer and generally smaller (Fig. 9C). Chlorophyll was low (0.37 Ixg/1) north of King
George Island where, again, there were few larvae (Fig. 4C).
Direct Observations of Development Results of the experimental observation of development of calyptopis stage 3 to furcilia stage 1 are shown in Table 4. By the end of the 5.3-day experiment, 75°70 of the larvae had molted. Morphology of the freshly molted larvae indicated that development tended to follow a direct pathway of development during the experiment, where molting produced a form having a full complement of 5 non-setose pleopods. The proportion of larvae having only 4, 3 or 2 pleopods did not increase significantly with time. We do not know whether or not those individuals which developed stunted pleopods (5'R, 4'R) would require an additional instar for development of full-sized pleopods. Chlorophyll concentration at the beginning of the experiment was 3.6 ~tg/1 and diminished to 0.94 txg/1 after 5
Table 4. Euphausia superba larvae: molting experiment. Stage 3 calyptopis larvae were placed in 10-1 carboys containing natural particulate matter. At the time intervals indicated, we emptied a carboy and counted the n u m b e r of larvae which had molted. Subdivisions of furcilia larvae indicate the n u m b e r of pleopods present; (R) indicates that all pleopods were reduced in size (smaller than usual) Elapsed time (h)
No. of. calyptopis 3
No. o f furcilia 1
12 36 55 71 89 108 127
49 42 31 29 28 19 9
0 7 10 18 9 30 19
5'
5' (R)
4'
4' (R)
3'
2'
0 0 0 0 3 0 4
0 1 2 1 2 1 4
0 0 0 0 0 2 0
0 0 0 1 1 0 0
0 0 0 0 2 0 0
Total nos.
% molted
°70 indirect pathway
49 50 43 49 45 52 36
0 16 28.1 40.8 37.7 63.5 75.0
0 12 16 I0 29 9 15
231
4.ot
100 u
r2 =0.85
3.0
,/ tJA
C~50 2.0
I D_ 0 Od
h-E
u
S -r
TIME (d)
I.O
Fig. 12. Molting rate of calyptopis stage 3 larvae to furcilia stage 1 maintained in natural particulate matter. Both larvae and particulate matter were collectedat a station in the eastern Scotia Sea
o
,,
~.
~
~
TIME (d)
Fig. 10. Decreasein chlorophylla (gg/l) during a 5-day experimentto determine the developmentrate of stage 3 calyptopis larvae days (Fig. 10). A linear regression explained 85o7o of the variance in the plot of chlorophyll versus time (i.e., r 2 = 0.85), indicating that the decline in chlorophyll concentration was more or less steady. We interpret this decrease to have been due primarily to grazing by the larvae, since there was no significant change in the chlorophyll concentration of the control (without larvae) over the same time period.
°FH 25 0
12h
~NN~ 56h
25 O
°fM
55h
25 0
71h
~ 25 ~
o
The gut fullness of larvae at each sampling interval during the experiment is shown in Fig. 11. For the first three days (up to, and including, 71 h) larvae showed the same trend: approximately 75°7o of the larvae had at least some material in their guts, with 30 to 50% having their guts at least half full. However, in the three samples taken during the final two days of the experiment the maj ority of larvae had empty guts, indicating reduced feeding. Chlorophyll concentrations during the last two days of the experiment were as high as 2 gg/1, which would be considered a "high" concentration in the Antarctic Peninsula region (e.g. Uribe 1982; Lipski 1982). Thus, a plausible explanation for the low gut contents of larvae at the end of the experiment is that only small phytoplanktons remained - phytoplankton which were too small to be efficiently ingested by the larvae. The development rate of larvae was calculated as the slope of the regression line of percentage of larvae molted versus time (Fig. 12). Molting rate remained constant throughout the experiment, despite clear changes in the feeding activity of the larvae. The calculated development rate from calyptopis stage 3 to furcilia stage 1 was 0.54o70/h, which corresponds to a development time of 7.7 days.
89h
Discussion o 5o
¢ 7~ f o u_ O
25
g
108h
,ool 5O 25
O
127h
75
5O 25 0
0
25 50 75 I00
% OF GUT FULLNESS
Fig. 11. Gut fullness of larvae during development rate experiment. For the last three days of the experiment most animals had empty guts
These data show that production of larvae of E. superba was at a low rate in February to March 1984 in the area investigated, particularly near Elephant Island and the South Shetland Islands. There, larvae were two orders of magnitude less abundant than had been found in 1981. Nevertheless, most 1984 larvae were pursuing direct developmental pathways, indicating now favorable conditions. The predominance of calyptopes over furciliae suggests that significant recruitment in 1984 may only just have been initiated by March in this area. Alternatively, J a n u a r y - February spawning was confined to other sectors of the Antarctic, or many larvae produced earlier in the Atlantic sector may have died or drifted out of the area. The near-absence of older furcilia
232
stages tends to discount the latter possibilities. Substantial numbers of larvae at the more eastern localities in the Scotia Sea indicate that environment was not uniform with respect to its ability to support reproduction and/or recruitment. Larvae emerging from hatching depths in the eastern part of the Scotia Sea appear to have been either (1) more abundant there than toward the west or (2) encountering conditions more suitable for survival there. Our experimental determination of the development time of stage 3 calyptopis to stage 1 furcilia (7.7 days) compares favorably with previous estimates. Based on field collections, Brinton and Townsend (1984) gave an estimate of 8 days. Ikeda (1984) found that larvae raised in the laboratory on a combination of Artemia larvae and Phaeodactylum required 9 days for this same period of development. These estimates are all approximately one half the maximum times reported by Witek et al. (1980), which were based on field samples. The proportion of calyptopis 3 larvae molting to furcilia 1 with a full complement of nonsetose pleopods (5') varied from 71 to 81% during the experiment. The proportion molting to furcilia 1 with 4' varied from 5 to 16%. These values are similar to those from the quantitative field sample (Sta. P-2) from the same locality at which the experimental animals were obtained: 75°7o of furcilia 1 with 5' and 17°70 with 4 ' . The absence of a clear trend toward indirect pathways of development as the experiment progressed suggests that diminishing food supply (leading to reduced feeding) may not, here, be a "poor environmental condition" causing multiple molts within stages in the sense of Makarov (1974). The experiment yielded the most interesting observation that - despite a clear decrease in feeding activity development rate remained constant. During the first three days of the experiment, many larvae had full guts and 50 to 75% had at least some material in their guts. However, during the final two days of the experiment, most of the larvae had no material in their guts, while the development rate remained constant. Thus, food supply and development rate of E. superba larvae may be independent for a period of at least several days. If longer development times do occur, as suggested by the field data of Witek et al. (1980), they might be due to chronic (rather than sporadic) food shortage. Evidence that recruitment was both "late" and generally of a low order in 1984 compared with 1981 may be summarized as follows: (1) March calyptopes were generally few, but far outnumbered furciliae; (2) older furciliae were almost absent; (3) furciliae were generally smaller than would have been expected if the February environment had been favorable for production and growth, but (4) calyptopes in most regions were not stunted, indicating recent improvement in the environment. (5) The prevailing use of relatively direct developmental pathways of larval development further supports the likelihood that conditions for growth were, by March, favorable.
Results of studies of juvenile and adult"Z?, superba from 1984 will be reported separately. However, it may be noted here that (1) a greater proportion of the non-larval krill were in the small size range of 20 to 30 mm in March 1984 than in Match 1981, possibly deriving from larvae produced late (March, April) in 1983 (see Table 1, 1983 observations), while (2) the largest 1984 krill, 48 to 55 ram, though not nearly as numerous as in 1981 and not forming large swarms, were almost entirely confined to waters west of Elephant Island and north of the South Shetlands near 60°W. Of these larger krill, almost all females were gravid, providing more evidence for a late spawning in 1984. Most smaller adults, there and in the other study areas, showed no evidence of reproductive activity, while a few appeared spent. Three particularly noteworthy aspects of the environment will be considered in detail in other reports: (1) water temperature in the 0 - 100 m layer north of the South Orkneys and Elephant Island, was up to 1 °C warmer in March 1984 than in March 1981, possibly indicating prolongation of the summer season, for example, Surface NW of S. Orkneys, 59°S, 50°W 25 Jan. 1981 1.45 t o l . 6 5 ° C 18 Mar. 1981 0.75 °C 8 Mar. 1984 1.44°C Elephant I., N side 7 - 2 2 Mar. 1981 0.1 to 0.5°C 17 - 19 Mar. 1984 1.1 to 1.2°C
100 m
- 0 . 1 5 to - 0 . 2 ° C - 0.2 °C 0.6°C
O.I°C 1.O°C
(1981 data from T. D. Foster; 1984 from D. E. Lange). (2) Salps, mainly Salpa thompsoni, were abundant in all regions studied in 1984 - commonly at 1 to 21 volume per 1000 m 3 of water, as had also been the case earlier in the season, (November - December 1983) east of the South Orkneys (Brinton •984). In 1981, salps were absent from most areas investigated. (3) 1984 chlorophyll a values were generally in the lower range of values found in 1981. It is not to be expected, of course, that high chlorophyll a will coincide for long with high densities of consumers; consumption rate rarely stays balanced by local primary production. Above some level of zooplankton biomass, feeding is limited. The extensive fields of dense E. superba larvae ( > 5 0 0 / m 3) northwest of the South Orkneys in 1981 appeared to have reduced ambient chlorophyll a from lateJanuary levels of near 2 ~tg/1 to 0.1 ~tg/1 by mid-March (Table 3), but the small body sizes of all larval stages suggested that growth had slowed well before our 17 March time of sampling. No such concentrations of krill larvae were found in 1984. Larvae of the two other important antarctic euphausiids, Thysanoessa macrura and Euphausia frigida, were also few in our 1984 samples from all areas; com-
233
pared with 1981. The commonly low values of chlorophyll a in 1984 (Table 3) seem not to have developed solely due to grazing. For example, low feeding rates measured for the ubiquitous 1984 salps (Huntley et al. 1984), together with their extremely low dry-weight to wetweight ratio (Marin et al. 1984) seem to limit the possibility that they are the consumers which controlled phytoplankton stocks. We described in the introduction how, of the 11 years between 1965 and 1983 for which there is relevant data from the Scotia and adjacent seas, three (1967, 1978, and 1983) seem to have been particularly poor for krill reproduction. The apparently late and low level of production of krill larvae in early 1984, though possibly turning for the better by mid-March, requires that there be continued examination of recruitment and production in relation to environmental events. Acknowledgements. We valued the cooperation and assistance of the personnel of R VMelville, of chief scientist E. Shulenberger, and of T. Antezana, J. Green, C. Jerde, P. Sykes and V. Marin, who were essential participants in our work on shipboard. This project was supported by the National Science Foundation, Grant DPP-8219147, a grant from the Smithsonian Institution's National Oceanographic Sorting Center, and by the Marine Life Research Program, the Scripps Institution's component of the California Cooperative Oceanic Fisheries Investigations.
References Brinton E (1984) Observations of plankton organisms obtained by bongo nets during the November-December 1983 Ice-Edge investigations. Antarct J US 4:113-115 Brinton E (1985) The oceanographic structure of the eastern Scotia Sea. 3. Distributions of euphausiid species and their developmental stages in relation to hydrography in 1981. Deep-Sea Res Brinton E, Antezana T (1984) Structures of swarming and dispersed populations of Krill (Euphausia superba) in Scotia Sea and South Shetland waters during January - March 1981, determined by bongo nets. J Crust Biol 4:45-66 Brinton E, Townsend AW (1984) Regional relationships between development and growth in larvae of Antarctic krill, Euphausia superba, from field samples. J Crust Biol 4:224-246 Fevolden SE (1980) Krill off BouvetOya and in the southern Weddell Sea with a description of larval stages of Euphausia crystallorophias. Sarsia 65:149-162 Fevolden SE, George RY (1984) Size frequency pattern of Euphausia superba in the Antarctic peninsula waters in the austral summer of 1983. J Crust Biol 4:107-122 Foster TD, Middleton JH (1984) The oceanographic structure of the eastern Scotia Sea. 1. Physical oceanography. Deep-Sea Res 31:529 - 550 Fraser FC (1936) On the development and distribution of the young stages of krill (Euphausia superba). Discovery Rep 14:1 - 1 9 2 George RY (1984) Ontogenetic adaptations in growth and respiration of Euphausia superba in relation to temperature and pressure. J Crust Biol 4:252- 262 George RY, StrOmberg J-O (1985) Development of eggs of antarctic krill Euphausia superba in relation to pressure. Polar Biol 4:125 - 133 Hempel I (1981) Euphausiid larvae in the Scotia Sea and adjacent waters in summer 1977/78. Meeresforsch 29:53 - 59 Hempel I (1985a) Variation in geographical distribution and abundance of larvae of antarctic krill, Euphausia superba in the southern
Atlantic Ocean. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin Heidelberg, pp 304 - 307 Hempel I (1985 b) Vertical distribution of larvae of antarctic krill, Euphausia superba. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin Heidelberg, pp 308-310 Hempel I, Hempel G (1978) Larval krill (Euphausia superba) in the plankton and neuston net samples of the German Antarctic expedition 1975/76. Meeresforsch 26:206- 216 Hempel I, Hempel G, Baker AC de (1979) Early life history stages of krill (Euphausia superba) in Bransfield Strait and Weddell Sea. Meeresforsch 27:267 - 281 Huntley ME, Barthel KG, Star JL (1983) Particle rejection by Calanus pacificus: discrimination between similarly sized particles. Mar Biol 74:151 - 160 Huntley M, Marin V, Sykes P, Rohan S (1984) Antarctic salps. 2. Trophodynamics. EOS, Trans Am Geophys Un 65:922 Ikeda T (1984) Development of the larvae of the Antarctic krill (Euphausia superba Dana) observed in the laboratory. J Exp Mar Biol Ecol 75:107 - 117 Ikeda T, Dixon P (1982) Body shrinkage as a possible over-wintering mechanism of the antarctic krill, Euphausia superba Dana. J Exp Mar Biol Ecol 62:143 - 151 Jackowska H (1980) Krill monitoring in Admiralty Bay (King George Island, South Shetland Islands) in summer 1979/1980. Polish Polar Res 1:117- 125 Jazdzewski K, Dzik J, Porebski J, Rakusa-Suszczewski S, Witek Z, Wolnomiejiski N (1978) Biological and populational studies on krill near South Shetland Islands, Scotia Sea and South Georgia in the summer 1976. Pol Arch Hydrobiol 25:607 - 631 Kikuno T (1981) Spawning behavior and early development of the Antarctic krill, Euphausia superba Dana, observed on board R VKaiyo Maru in 1979/80. Antarct Rec, Tokyo 73:97- 102 Kittel W, Jazdzewski K (1982) Studies on the larval stages of Euphausia superba Dana (Crustacea, Euphausiacea) in the southern Drake Passage and in the Bransfield Strait in February and March 1981 during the BIOMASS-FIBEX expedition. Polish Polar Res 3:273- 280 Knight MD (1984) Variation in larval morphogenesis within the Southern California Bight population of Euphausia pacifica from winter through summer, 1977 - 1978. Calif Coop Oceanic Fish Invest Rep 25:87-99 Lipski M (1982) The distribution of chlorophyll-a in relation to the water masses in the southern Drake Passage and Bransfield Strait (BIOMASS-FIBEX, February-March 1981). Polish Polar Res 3:143 - 152 Mackintosh NA (1972) Life cycle of Antarctic krill in relation to ice and water conditions. Discovery Rep 36:1 - 94 Makarov RR (1972) The life history and peculiarities of the distribution of Euphausia superba Dana. Tr Vses Nauchno-Issled Rybnogo Okeanogr 77:85 - 92 Makarov RR (1974) Larvae of Euphausia superba Dana in plankton from the Sea of Scotia. Tr Vses Nauchno-Issled Rybnogo Okeanogr 99:84 - 103 Makarov RR, Maslennikov VV (1981) Ecology of larval development of the crustacean Euphausia superba. Change in dominant larval forms as a function of environmental conditions. Mar Ecol Prog Set 4:265 -271 Marin V, Huntley M, Sykes P, Rohan S (1984) Antarctic salps. 1. Biomass, distribution and biometry. EOS, Trans Am Geophys Un 65:922 Mart JWS (1962) The natural history and geography of the Antarctic krill (Euphausia superba Dana). Discovery Rep 32:33 - 464 Marschall H-P (1983) Sinking speed, density and size of euphausiid eggs. Meeresforsch 30:1 - 9 Marschall H-P (1984) Development, swimming and feeding of early stages of krill. Antarct J US 19:137-138 Marschall H-P, Hirche H-J (1984) Development of eggs and nauplii of Euphausia superba. Polar Biol 2:245 - 250 Marschall S, Mizdalski E (1985) Euphausiid larvae in plankton samples
234 from the vicinity of the Antarctic Peninsula, February 1982. Beri Polarforsch 21:1 - 47 McWhinnie MA, Denys CJ (1978) Biological studies of antarctic krill, austral summer, 1977- 1978. Antarct J US 13:133 - 134 Miller C, Huntley M, Brooks E (1984) Post-collection molting rates of planktonic, marine copepods: measurement, applications, problems. Limnol Oceanogr 29:1274- 1289 Nast F (1979) The vertical distribution of larval and adult krill (Euphausia superba Dana) on a time station south of Elephant Island, South Shetlands. Meeresforsch 27:103-118 Quetin LB, Ross RM (1984a) School composition of the antarctic krill Euphausia superba in the waters west of the antarctic peninsula in the austral summer of 1982. J Crust Biol 4:96-106 Quetin LB, Ross RM (1984b) Depth distribution of developing Euphausia superba embryos, predicted from sinking rates. Mar Biol 79:47 - 53 Rakusa-Suszczewski S (1984) Krill larvae in the Atlantic sector of the Southern Ocean during FIBEX 1981. Polar Biol 3:141 - 147 Rakusa-Suszczewski S, Stepnik R (1980) Three species of krill from
Admiralty Bay (King George, South Shetlands), in summer 1978/79. Pol Arch Hydrobiol 27:273- 284 Reeve MR (1981) Large cod-end reservoirs as an aid to the live collection of delicate zooplankton. Limnol Oceanogr 26:577- 579 Ross RM, Quetin LB (1982) Euphausia superba: fecundity and physiological ecology of its eggs and larvae. Antarct J US 17:166 - 167 Stein M, Rakusa-Suszczewski S (1984) Meso-scale structure of water masses and bottom topography as the basis for krill distribution in the South Eastern Bransfield Strait, February - March 1981. Meeresforsch 30:73 - 81 Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, 2nd edn. Bull Fish Res Board Can 167:1- 310 Uribe E (1982) Influence of the phytoplankton and primary production of the Antarctic waters in relationship with the distribution and behavior of krill. Inst Antarct Chileno, Sci Ser 28:147 - 163 Witek Z, Koronkiewicz A, Soszka GJ (1980) Certain aspects of the early life history of kriU Euphausia superba Dana (Crustacea). Pol Polar Res 1:97-115
