Oxford University Press Journal of Plankton Research Vol.16 no.ll pp , 1994

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1 Journal of Plankton Research Vol.16 no.ll pp , 1994 Life cycle strategies and seasonal variations in distribution and population structure of four dominant calanoid copepod species in the eastern Weddell Sea, Antarctica S.B.Schnack-Schiel and W.Hagen 1 Alfred-Wegener-Institut fur Polar- und Meeresforschung, Columbusstrasse, D Bremerhaven and 'Institut fur Polarokologie, Universitdt Kiel, Wischhofstrasse 1-3, Gebdude 12, D Kiel, FRG Abstract. The dominant Antarctic copepod species Calanoides acutus, Calanus propinquus, Rhincalanus gigas and Metridia gerlachei were investigated with respect to their abundance, vertical distribution, developmental stage composition, dry weight and lipid content. The specimens were sampled during three expeditions to the eastern Weddell Sea in summer (January/February 1985), late winter/early spring (October/November 1986) and autumn (April/May 1992) between 0 and 1000 m depth to follow the seasonal development of the populations. Three species were most abundant in April, only C.propinquus reached highest concentrations in February. A seasonal migration pattern was evident in all four species, but was most pronounced in C.acutus. In October/ November, they inhabited deeper water layers, their ascent started by mid-november and in mid- February the species concentrated in the upper 50 m, except for M.gerlachei ( m). Their descent was observed in April/May. The stage composition changed dramatically with season, the older developmental stages (CIII-CVI) dominated the populations in late winter/early spring, whereas younger stages (CI and CII) prevailed during summer (C.acutus, C.propinquus) or autumn (R.gigas, M.gerlachei). Only C.acutus ceased feeding in autumn and diapaused at depth. Strong differences between seasons were also detected in dry weight and lipid levels, with minima in late winter/early spring and maxima in summer {C.acutus, R.gigas) or autumn (C.propinquus, M.gerlachei). Lipid reserves seem to be most important for the older stages of C.acutus and C.propinquus. Based on these seasonal data, different life cycle strategies are suggested for the four species. Introduction Zooplankton biomass in the Southern Ocean is usually dominated by the four large calanoid copepod species Calanoides acutus, Calanus propinquus, Rhincalanus gigas and Metridia gerlachei (e.g. Chojnacki and Weglenska, 1984; Boysen-Ennen etal., 1991; Hopkins etal., 1993). Data on their distribution and age composition were first given by Ottestad (1932, 1936), Ommanney (1936) and Andrews (1966). Many questions still remain, although our knowledge of the life histories of these species has improved considerably during the last few years (e.g. Marin, 1988; Atkinson, 1991; Huntley and Escritor, 1991, 1992; Schnack-Schiel etal., 1991; Bathmann etal., 1993; Drits etal., 1993; Hopkins et al., 1993). Calanoides acutus occurs in relatively high abundances in the entire Southern Ocean (Zmijewska, 1983; Hopkins, 1985a, 1987; Hubold and Hempel, 1987; Hopkins and Torres, 1988). Males occur only in deeper water layers in winter, where mating takes place. In spring, fertilized females ascend to the upper water layers to spawn and in summer the new generation thrives in the productive surface waters, while the older stages especially accumulate large lipid reserves in the form of wax esters (Hagen, 1988; Schnack-Schiel et al., 1991). In autumn, Oxford University Press 1543

2 S.B.Schnack-Schiel and W.Hagen feeding ceases and older copepodids descend to deeper water layers to overwinter in a resting stage (Andrews, 1966; Voronina, 1970; Hopkins, 1985b; Schnack-Schiel et al, 1991). Marin (1988) and Atkinson (1991) suggested a 1- year life cycle. Calanus propinquus generally prefers colder water masses and does not occur in high densities in the Antarctic Circumpolar Current (Bathmann et al., 1993). During summer, the population is concentrated in the surface layer, where it feeds, develops and replenishes its extensive lipid reserves, mainly triacylglycerols (Schnack-Schiel et al., 1991; Hagen et al., 1993). According to Marin (1988) and Bathmann et al. (1993), part of the C.propinquus population remains in surface waters during winter and continues to feed. In contrast to C.acutus, this species mainly mates in surface layers and males are present throughout the summer. In the eastern Weddell Sea, Fransz (1988) found small amounts of eggs and nauplii of C.propinquus very early in the season (October-November) with virtually no phytoplankton in the water column (Gieskes et al., 1987). Major spawning, however, is believed to take place in December [Kosobokova (1992), in Drits et al. (1993)]. Marin (1988) described a 1-year life cycle, but based on physiological and biochemical measurements, Drits et al. (1993) suggested a 2- year life cycle for C.propinquus. Rhincalanus gigas is a typical species of the Antarctic Circumpolar Current and is not very abundant in the Weddell Sea (Ottestad, 1932; Bathmann et al., 1993; Hopkins et al., 1993). Ommanney (1936) postulated that optimum spawning occurs between 1 and 4 C, but no spawning at temperatures <0 C, and Vervoort (1965) assumed no spawning in the Weddell Sea. However, according to Bathmann et al. (1993), R.gigas reproduces in the Warm Deep Water of the eastern Weddell Sea in autumn. Late autumn spawning was also described by Marin and Schnack-Schiel (1993) in the Antarctic Peninsula region, although in surface waters. According to Atkinson (1991), the spawning period of R.gigas extends over a longer period with the main activities in spring and autumn. The heterogeneous data indicate that R.gigas has a more flexible, 1- or 2-year life cycle, probably depending on latitudinal influences (Marin, 1988; Atkinson, 1991; Bathmann et al., 1993). Metridia gerlachei is one of the most numerous calan,oid species in Antarctic waters (e.g. Schnack et al., 1985; Zmijewska, 1985; Boysen-Ennen and Piatkowski, 1988; Hopkins and Torres, 1988), although in spite of its ubiquity very little is known about its life history. Vervoort (1965) suggested that M.gerlachei spawns at the end of the austral summer. However, data by Zmijewska (1987) and Huntley and Escritor (1992) indicate the onset of breeding earlier in the season. Spawning in the Antarctic Peninsula region was more or less continuous from November to January and two or three generations may be produced during one summer period (Huntley and Escritor, 1992). Metridia gerlachei does not seem to undergo ontogenetic vertical migrations (Atkinson and Peck, 1988) and no massive lipid depots are accumulated during summer (Hagen, 1988; Graeve et al., 1994). The present study summarizes results obtained during three expeditions to the eastern Weddell Sea in late winter/early spring, summer and autumn. Based on 1544

3 Life cycle strategies of calanoid copepods distribution pattern, age structure, dry weight and lipid data, we tried to elucidate the different life cycle strategies of these four copepod species and their adaptations to the pronounced seasonality of ice cover, light regime and primary production in high-antarctic waters. Method Copepods were sampled in the eastern Weddell Sea during three Antarctic expeditions with RV 'Polarstern': ANT III/3 in January/February'1985, ANT V/ 3 in October/November 1986 and ANT X/3 in April/May 1992 (Figure la and b). Samples were collected at five depth strata from 1000 m to the surface using a multiple opening-closing net system fitted with 100 xm mesh nets. The depth layers were chosen according to the vertical structure of the hydrographic regime. During ANT III/3 and ANT V/3, the filtered volume was calculated based on the vertical distance covered by the net's mouth area (0.25 m 2 ), assuming 100% efficiency. During ANT X/3, the multi-net was equipped with a digital flowmeter. Samples were preserved in 4% buffered formaldehyde and analysed for abundance, distribution and age structure. According to density, samples were split into subsamples (1/2-1/32) using a Kott whirling apparatus or a Folsom splitter. Geometric means were applied for comparison between sampling periods. The mean population stage [S] was calculated after Marin (1987). For dry weight and lipid analyses, the specimens were carefully collected by Bongo net, and live copepods were immediately sorted to species and stages in a cooling container at 4 C. A single sample usually comprised between 50 and 200 specimens, which were stored in a glass vial at -80 C. After freeze-drying for 48 h and dry weight measurements in the home laboratory, lipids were extracted with chloroform:methanol (2:1, v:v) and the lipid content as percent of dry weight (%DW) was determined gravimetrically after Folch et al. (1957). Results Calanoides acutus Overall abundance of C.acutus changed significantly between seasons (//-Test, 95% level). In October/November and late January, the abundance was ~2 individuals (ind.) m~ 3, but increased dramatically towards mid-february (7 ind. m~ 3 ) and mid-april (9 ind. m~ 3 ). At the end of April, C.acutus again decreased in abundance and with 3 ind. m~ 3 it was only slightly higher than in October- January (Figure 2a). During late winter/early spring, older copepodite stages (CIV and CV in mid- October, CIV and females in November) dominated the population (Figure 2b), whereas the youngest stages (CI and CII) were not encountered. At the end of January, the stage distribution was bimodal with major concentrations of CI, CII and CV specimens. In mid-february, CI and CII stages formed the bulk of the population with 55 and 25%, respectively. In autumn, older stages (CIV and CV) comprised >95% of the population, whereas CI specimens were not 1545

4 S.B.Schnack-Schiel and W.Hagen 70 60" 50 40' 30" (a) 73 20' W 22* " 12" 11* 10* 9" 8" 7" 6"W Fig. 1. Investigated area and locations of sampling stations (a, b) during three 'Polarstern' expeditions, (a) ANT III/3 (January/February 1985) and ANT V/3 (October/November 1986); (b) ANT X/3 (April/May 1992). encountered and CII was rare in mid-april (0.2% of the population) (Figure 2b). The population was oldest in late winter/early spring and youngest in mid- February (mean population stage [S] 5 and 2, respectively; Figure 2c). Adults made up between 39 and 50% of the population in late winter/early spring, 1546 (b) 68 69" 70"

5 Calanoides acutus Life cycle strategies of calanoid copepods late winter/early spring 1986 summer 1985 autumn 1992 (a) 12 sr io E 8 3. I 6H i 4 " ^ October November Ratio 1.0 : 1.1 : 0.9 (b) 10 - (C) IS] January February i April April 2. May 0.8 : : 1.6 imales DFemales BCV DCIV QCm HCII DDCI no CS no CS no CT no (7 Fig. 2. Total abundance (a) and relative abundance of developmental stages (b), mean population stage [S] and female:male ratio (c) of C.acutus. whereas in summer and autumn their proportion comprised only 3-6%. Females always outnumbered males, which were only found in winter/spring. In mid-october, ~80% of the population was located in the Warm Deep Water between 1000 and 500 m (Figure 3). Towards mid-november, there was a gradual migration into upper water layers (Figure 3) and the population became older due to the ascent of fertilized females. In mid-october, <1% of the 1547

6 S.B.Schnack-Schiel and W.Hagen late wtnterlearly spring 1986 summer 1985 autumn IS AprU- Oclok Nwcmber November JpmrPy Febnray 2 May Rtlatlvc abundance (%) Fig. 3. Vertical distribution of C.acutus as a percent of total numbers and temperature profile within the upper 1000 m. population occurred in the top 50 m, whereas in mid-november this proportion had increased to 9%. In summer, the majority concentrated in the warm surface layer with 62% at the end of January and 90% in mid-february, mainly offspring of the new generation. The depth distribution in autumn was bimodal with a smaller fraction in the upper 90 m and a larger one in the Warm Deep Water layer. The developmental structure differed with depth, a younger fraction (CIII, CIV: 80-90%) was encountered in the surface layer and an older one in the deepest water layer (CIV, CV: 95%). During October/November, the dry weight of C.acurus increased from 127 ~g in stage CIV and 195 kg in CV to the adult stages (579 kg in females and 606 kg in males). The available summer data showed much higher dry weights of CV stages (729 pg) and femaies (909 ~ g), which were very similar to the autumn dry weights (CV: 755 pg; females: 899 kg). In autumn, stage CIII weighed 69 pg and CIV 187 pg (Figure 4a). In late winterlearly spring, lipid contents increased from stage CIV (12%DW) and CV (14%DW) to females (32%DW) and males (37%DW). Lipid levels were even higher in summer, with 45%DW in CV stages and 48%DW in females. In autumn, lipid contents were quite high in stages CIII (32%DW) and CIV (26O/oDW), while in CV and females (both 45%DW) lipid contents were very similar to the summer data. This lipid accumulation may at least partially explain the higher dry weights in summer and autumn (Figure 4b). Calanus propinquus Calanuspropinquus occurred with -1 ind. m-3 in the upper 1000 m in October1 November and at the end of January. Two weeks later, in mid-february, abundance peaked with -6 ind. ma3 and in autumn the population was recorded with -4 ind. m-3 (Figure 5a). In mid-october, copepodite stages CIII, CV and females formed 84% of the population (Figure 5b). Towards mid-november, the proportion of CIII increased, while that of females decreased. At the end of January, the population structure was bimodal, dominated by the youngest (CI) and the oldest (CV and females) stages. In mid-february, the C.propinquus population was represented mainly by CI copepodids (63%), whereas in autumn the

7 Life cycle strategies of calanoid copepods 1400 Calanoides acutus a Q o D. 1 Fig. 4. Dry weight (a) and total lipid content (b) of C.acutus; number of error bars = number of samples examined. copepodite stages CIII-CV dominated with 90% (Figure 5b). The mean population stage changed only slightly during the late winter/early spring period. At the end of January, the population was about one copepodite stage younger and in mid-february more than two stages younger than in mid-november. In autumn, the population was again older with an intermediate mean population stage (Figure 5c). In late winter/early spring, adults represented between 20 and 30% of the population, whereas in summer and autumn they accounted for only 2-7%. Males occurred in higher numbers only in October/November; they were missing in autumn (Figure 5c). In October/November, the major part of the population inhabited the layer between 500 and 200 m (Figure 6). From mid-october to mid-november, there was an increase in abundance in upper water layers, mainly due to the ascent of CIII specimens. During all three sampling periods in late winter/early spring, 10-16% of the population was concentrated in the top 50 m. In summer and autumn, the majority of the population was located in this layer. The October/November data for C.propinquus showed an increase in dry weight from 52 u.g in stage CIII, 157 u.g in CIV, 773 jig in CV to 887 u.g in males and 1158 u.g in females. The summer dry weights ranged from 79 u.g in CII to 1692 u,g in females. Hence, dry weights of C.propinquus were clearly higher in summer as compared to the corresponding late-winter stages, only in the males 1549

8 S.B.Schnack-Schiel and W.Hagen (a) (b) (C) u T3 late winter/early spring October November Calanus propinquus summer January February autumn April April 2. May n- rh Ratio ioo IS] Q'Cf i Males D Females SCV QCIV racill HCH no Cf Fig. 5. Total abundance (a) and relative abundance of developmental stages (b), mean population stage [S] and female:ratio (c) of C.propinquus. was the difference not as pronounced. In autumn, dry weights ranged from 21 u,g in stage CII to 1640 u.g in females. They were somewhat lower than during summer, especially in stages CIII (69 u.g) and CV (814 u.g) (Figure 7a). The available lipid data from October/November showed a strong increase in total lipid content from CIII and CIV (19 and 16%DW, respectively) to CV (33%DW), but lipid contents decreased again in the adult stages (females:

9 Life cycle strategies of calanoid copepods late winter/early spring *. October November November SO SO r -r (re Ccdanus propinquus summer IS. Januaiy February Relative abundance (%) ao o u 40 n ao o GO ao autumn April- April 2Mzy ao ao 0 xo 40 ao ao Fig. 6. Vertical distribution of C.propinquus as a percent of total numbers and temperature profile within the upper 1000 m Ccdanus propinquus Fig. 7. Dry weight (a) and total lipid content (b) of C.propinquus; number on error bars = number of samples examined. 26%DW; males: 28%DW). In summer, copepodite stages CII (18%DW) and CIII (21% DW) had moderate lipid levels. Maximum values were reached in the CV stages (39%DW), which decreased again in the females (35%DW) and especially in the males (24%DW). Lipid levels were generally higher during summer and autumn, except for the males. The variability in lipid content was strongest in stages CV and females (Figure 7b). 1551

10 S.B.Schnack-Schie! and W.Hagen Rhincalanus gigas Rhincalanus gigas was generally encountered in low densities and reached maximum abundance in mid-april (0.4 ind. m~ 3, Figure 8a). During late winter/ early spring, the population was mainly represented by older copepodite stages (CIII-CV) and females (Figure 8b). The relative abundance of CIV gradually decreased throughout late winter/early spring, while that of stages CIII and CV Rhincalanus gigas (a) <n U c 3 late winter/ early spring 1986 summer October November January February autumn April April 2. May 0 Ratio : V u I 3 <u rt (C) 60 20H IS) 9-CT v,v,v WAV VvV>V / / / / / T I Males OFemales BCV QCIV E3CIII DCII QBCI T ' _. Fig. 8. Total abundance (a) and relative abundance of developmental stages (b). mean population stage [5] and female:male ratio (c) of ft.gigas. 1552

11 Life cycle strategies of calanoid copepods increased. Copepodite stage CII and males made up only 1-3% of the population, and CI specimens did not occur in the samples. At the end of January, the mean population stage [5] was one copepodite stage younger than in mid-november (Figure 8c), and stages CII and CHI clearly prevailed with 20 and 50%, respectively. Two weeks later, in mid-february, the population had become older with CIII and CIV comprising 50 and 22%. As in late winter/early spring, no CI specimens were encountered during summer. In mid-april, the stage distribution was bimodal: CI and CII accounted for 37%, CV and adults for 49%. The relative frequency of CI decreased from mid-april to the end of April, when the CV fraction increased. Only in autumn were high abundances of R.gigas nauplii found in the upper water layers. They comprised an average of 36% of the total surface population in mid-april, but only 8% 2 weeks later (S.B.Schnack-Schiel, unpublished data). Adults made up a large fraction of the population during all sampling periods (15-32%). Females were always found in much higher numbers than males, except at the end of January (Figure 8c). In late winter/early spring, the bulk of R.gigas inhabited the depth layer between 500 and 200 m, i.e. the transition layer between the cold Winter Water and the Warm Deep Water (Figure 9). A considerable portion of the population (21-39%) was also found in the deepest water layer investigated, the Warm Deep Water. In summer, the majority of the population was restricted to the upper 100 m. At the end of January, >90% were encountered in the cold layer of the Eastern Shelf Water ( m), whereas in mid-february only 23% inhabited this depth strata and 72% ascended into the warm surface layer (50-0 m). In mid-april, R.gigas showed a bimodal depth distribution. The majority of the population (69%) occurred in the cold upper water layers and consisted almost entirely of stages CI and CII (98%). Below 330 m, 29% of the population were encountered. The oldest copepodite stages (CIV and CV) had their maximum distribution between 330 and 200 m, whereas the females were concentrated below 330 m. At the end of April, only a small fraction of the population was found in the surface layer. The majority occurred between 150 and 90 m, and below 330 m. Stages CI and CII had descended, and occurred in highest numbers between 230 and 90 m. Later copepodids and females again inhabited deeper layers than the earlier stages. aoo- o- i [ O- late winter/early spring October November November B 0 0 2O 40 6O SO 0 3 O 4 0 I / : Rhincalanus gigas summer 19S Januajy Pebruaiy Relative abundance (%) ao.o JO «o oo ao o» «tt n autumn April 28. Aprtl- 2 May 0» 40 SO 00 0 X M 60 N Fig. 9. Vertical distribution of R.gigas as a percent of total numbers and temperature profile within the upper 1000 m. 1553

12 S.B.Schnack-Schiel and W.Hagen Dry weights of R.gigas during late winter showed a steady increase between stages, from CIII (114 ng), CIV (316 u.g), CV (763 u.g) to males (1041 u,g) and females (1365 u,g). Dry weights of the CIII (136 y-g) and CIV (329 u.g) specimens from summer were slightly higher than the corresponding winter/ spring stages. During summer, CV specimens (1117 o,g) and females (1722 fig) were clearly heavier, and in autumn CV stages (1267 u,g) further increased in weight, while females were again lighter (1575 u,g). Dry weights were in a similar range as found for C.propinquus, but usually with a lower variability (Figure 10a). During late winter/spring lipid contents of R.gigas were moderate to low in stage CIII (20%DW), CIV (12%DW), CV (16%DW) and females (15%DW), and highest in the males (24%DW). In summer, lipid contents were generally higher, especially in stage CV (31%DW) and females (26%DW). These were similar to the autumn data with 25%DW in stage CV and 26%DW in females (Figure 10b). Metridia gerlachei The abundance of M.gerlachei did not differ much between October/November and January/February, with ~7-10 ind. m~ 3, but in autumn its abundance had tripled (Figure lla) Rhincalanus gigas cu cm civ cv F M Oct/Nov Jan/Feb Q] Apr/May Fig. 10. Dry weight (a) and total lipid content (b) of R.gigas; number on error bars = number of samples examined. 1554

13 Life cycle strategies of calanoid copepods Although overall abundance data varied only slightly in late winter/early spring and summer, a great difference in age structure was evident (Figure lib). CIII, CIV and females dominated in late winter/early spring. The proportion of CIV increased towards mid-november, while that of CII decreased. Stage CI Metridia gerlachei late winter/early spring 1986 summer 1985 (a) so a 20 c 3 < 10-0 Ratio (b) October isi November January February 1.0 : 0.7 : : Males DFemales MCV QCIV QCin QCH IfflCI autumn April - April 2. May 4.0 : Fig. 11. Total abundance (a) and relative abundance of developmental stages (b), mean population stage [5] and female:male ratio (c) of M.gerlachei. 1555

14 S.B.Schnack-Schiel and W.Hagen was almost absent (<0.2% of the population). In contrast, during summer the age structure was bimodal with Cl and adults dominating. In autumn, young copepodids (CI-CIII) made up >80% of the population. During late winter/ early spring and summer, adults accounted for 20-30% of the population, but for only 2% in autumn. Females were more abundant than males, except in autumn. The mean population stage [S] was about one copepodite stage younger in autumn than in summer and almost two stages younger than in late winter/ early spring (Figure lie). In mid-october, the bulk of the population was concentrated in the Warm Deep Water between 1000 and 500 m (Figure 12). Towards mid-november, the population was more dispersed between 1000 and 10 m. At the end of January, the majority had ascended to the layer between 300 and 100 m (65%), although a considerable part of the population (15%) was still encountered in the deepest water layer. In mid-february, 55% of the population were located between 100 and 50 m, but in mid-april the bulk (73%) were again found between 300 and 100 m. At the end of April, a larger fraction of the population had descended to deeper water layers ( m) and 19% of the population were found below 330 m. This species is by far the lightest of the four calanoids considered. The data for M.gerlachei from late winter/early spring show a strong increase in dry weight from stage CIV (21 p.g) and CV (54 u,g) to males (71 u.g) and females (256 u.g). Higher dry weights were determined in summer for CV stages (83 u,g) and females (326 u.g), and in autumn dry weights of CV stages (158 u.g) almost doubled, while those of the females (303 u,g) decreased slightly (Figure 13a). In late winter/early spring, maximum lipid levels were found in the males and CIV stages, although with 24%DW (CIV), 22%DW (CV) and 11%DW (females) M. gerlachei had rather moderate lipid contents. Similar lipid levels were found during summer for stage CV (21%DW), while those of the females (18%DW) were clearly higher, as compared with the earlier season. Lipid contents of females (25%DW) continued to increase in autumn, but a massive increase was determined for the CV stages (40%DW) (Figure 13b). Discussion The four species studied exhibit different seasonal patterns in abundance, vertical distribution, age structure and lipid levels. All species undergo seasonal vertical migrations, but they differ in their depth of maximum occurrence and their timing of reproduction. Calanoides acutus Our data on the vertical distribution and population structure of C.acutus in the eastern Weddell Sea corroborate the results from various Antarctic regions by Andrews (1966), Marin (1988), Atkinson (1991), Huntley and Escritor (1991), Schnack-Schiel et al. (1991), Bathmann et al. (1993), and Marin and Schnack- Schiel (1993), and verify that C.acutus is a strong ontogenetic seasonal migrant. In the Antarctic Peninsula area, Huntley and Escritor (1991) found the youngest 1556

15 Life cycle strategies of calanoid copepods late winter/earry spring October November November Metridia gerlachei summer 29. January Relative abundance (%) 1985 is. February autumn 1Z- 13. April 1992 M. April 2 May Fig. 12. Vertical distribution of M.gerlachei as a percent of total numbers and temperature profile within the upper 1000 m Q 100 Q i.! a (a) (b) CH Metridia gerlachei CHI Oct/Nov CIV CV H Jan/Feb F M Q Apr/May Fig. 13. Dry weight (a) and total lipid content (b) of M.gerlachei; number on error bars = number of samples examined. copepodite stage (CI) in December and they concluded that spawning must have started in October. Andrews (1966) suggested that egg production of C.acutus begins in November, but with peak activities in December and January. In the eastern Weddell Sea, Fransz (1988) did not find eggs and nauplii of C.acutus before the end of November. Males were only encountered in October/ November and only in deep water layers. During this period, females and males 1557

16 S.B.Schnack-Schiel and W.Hagen comprised about half of the population; hence, the main mating seems to occur at depth during October/November. In November, fertilized females ascended to the surface to spawn (Schnack-Schiel et al., 1991). Based on a developmental time from eggs to late nauplii of ~50-60 days, as Fransz (1988) reported for C.propinquus and M.gerlachei, CI specimens of C.acutus should occur by mid- January. Unfortunately, no data are available on the stage composition of C.acutus for December/early January in the eastern Weddell Sea. However, at the end of January 27% of the population consisted of CI specimens, which supports our above hypothesis on developmental time. This new generation was concentrated in the upper 50 m. Huntley and Escritor (1991) determined a mean stage duration time of 30 days for C.acutus copepodids in the Antarctic Peninsula area and in the Drake Passage. If we assume the same developmental rate for the eastern Weddell Sea, CIV specimens from the new generation should occur by mid-april, which is confirmed by our data (CIV: >60% in April). Copepodite stages CIV started their descent in April, and only CIV- CVI stages of C.acutus seem to overwinter in a resting stage below 500 m in the Warm Deep Water (Bathmann et al., 1993; Hopkins et al., 1993). In October/beginning of November, chlorophyll a concentrations in the water column were <0.02 u.g I" 1, and with the onset of ice melting in mid-november chlorophyll a increased to ~0.2 u-g P 1 (Scharek, 1991). In early spring, no feeding of CV stages and females of C.acutus could be detected when offering naturally occurring phytoplankton concentrations; however, feeding occurred in experiments with enriched food supply carried out at the end of November. Swimming and respiration activities of female C.acutus increased from October towards the end of November (Schnack-Schiel et al., 1991). These observations indicate changes in physiology and behaviour after 'awakening' from diapause and returning to the active state. In January/February, the mean chlorophyll a concentration was ~1 u,g I" 1 (Nothig et al., 1991). Feeding experiments in late January showed high grazing rates of copepodite stages CIII to females at ambient concentrations (Schnack-Schiel et al., 1991). In February, all developmental stages of C.acutus from the Ross Sea had food in their guts, and there was a change in diet with ontogeny from purely diatoms in late nauplii to a mixture of diatoms, dinoflagellates and protozoans in older stages (Hopkins, 1987). During April, chlorophyll concentrations varied between 0.1 and 0.3 u,g I" 1 in the upper water layers and below m the concentration decreased to 0.01 u,g P 1 (Spindler et al., 1993). Feeding experiments showed that in April all copepodite stages in the surface layer (CIII and CIV) were actively grazing on naturally occurring suspensions, whereas stage CV from the deepest water layer had ceased feeding, independent of the food concentrations offered, indicating the onset of diapause. Grazing rates of stage CIV from deeper waters varied considerably between experiments (from no feeding to very active feeding as found at the surface; S.B.Schnack-Schiel, unpublished data). Similar results were reported by Hopkins and Torres (1989) from the northwestern Weddell Sea, where in March C.acutus was actively feeding on phytoplankton and protozoans in the upper 200 m, while specimens from below 200 m had empty guts. 1558

17 Life cycle strategies of calanoid copepods The seasonal differences are also reflected in the dry weights and lipid levels of the various C.acutus stages. In late winter/early spring, these data are consistently lower than during the summer and autumn. As stated above, C.acutus overwinters (mainly as CIV and CV) in diapause at depth. Hence, the low dry weights and lipid contents in the CV stages early in the season may originate from recently moulted CIV stages, which have rather similar data. The interpretation of the female data is more complicated and somewhat blurred by the averages. We noticed specimens with large and with small oil sacs, and hypothesize that the occurrence of lighter, lipid-poor females may be explained by freshly moulted CV stages or energetic losses due to gonad formation (Gatten et al., 1980; Hagen et al., 1993; Hirche and Kattner, 1993). Since primary production in early spring was still at a minimum (Scharek, 1991), internal energy reserves were probably utilized to fuel reproduction and these specimens did not have the opportunity to replenish their lipid depots, mainly wax esters, through phytoplankton, in contrast to the summer stages. Calanus propinquus Our results from the eastern Weddell Sea show that in late winter/early spring the copepodite stages CIII, CV and females dominated. At this time of the year the adult population comprised ~20-30% and males were encountered in high densities, especially in November. In this region, Fransz (1988) already found C.propinquus eggs and nauplii in early October; hence, all these observations suggest that the main mating period is in late winter/spring. As in C.acutus, the new generation (CI, CII) of C.propinquus dominated the population during summer, and was concentrated in the upper 50 m. Similar results were also reported by Voronina (1978) and Marin (1988). In April, the C.propinquus population consisted mainly of stages CIII-CV in the eastern Weddell Sea, while CI and CII specimens made up <10%. In contrast, studies in the Scotia Sea by Hopkins et al. (1993) showed that CI and CII specimens comprised >20% of the population during mid-winter. Hence, reproduction time was shorter in the more polar eastern Weddell Sea, as compared to the Scotia Sea. On the other hand, the occurrence of eggs and nauplii in early October (Fransz, 1988), and of CI and CII stages in May (this study), suggests that C.propinquus reproduces over a more extended period in the eastern Weddell Sea than observed for C.acutus (Schnack-Schiel et al., 1991). In contrast to the deeper overwintering C.acutus, half of the C.propinquus population was located between 500 and 200 m in mid-october, which supports the findings by Vladimirskaya (1979). Similar to C.acutus, the C.propinquus population had started to ascend by mid-november, and during all three sampling periods in late winter/early spring only a relatively small portion of the population (10-16%) was encountered in the surface layer. In contrast, in September/October in the Weddeil Gyre Bathmann et al. (1993) found C.propinquus mainly concentrated in the top 200 m, in some cases even close to the surface, while a small fraction of this population was also collected in deeper waters down to 2000 m. A separation of the population into surface and deep- 1559

18 S.B.Schnack-Schiel and W.Hagen living specimens was also described by Marin (1988). Drits et al. (1993) found that C.propinquus individuals from deeper waters (>500 m) were richer in lipid and protein, and had lower respiration and excretion rates, as compared to specimens from the upper 100 m. Feeding studies in the Scotia Sea by Hopkins et al. (1993) and in the Weddell Gyre by Bathmann et al. (1993) proved that C.propinquus was actively feeding during the austral winter. In October/ November, in the southeastern Weddell Sea, Schnack-Schiel et al. (1991) found high respiration rates and swimming activities. Feeding experiments carried out in April in the eastern Weddell Sea showed C.propinquus actively feeding on phytoplankton (S.B.Schnack-Schiel, unpublished data). Examinations of the gut contents of C.propinquus during summer, autumn and winter revealed no differences in diet: during all seasons phytoplankton, protozoans and metazoans were ingested (Hopkins, 1985b, 1987; Hopkins and Torres, 1989; Hopkins etal., 1993). It is interesting that C.propinquus from the pack-ice region exhibited a significantly larger zooplankton fraction in their diet as compared to open-water specimens, a possible indication that C.propinquus benefits from the iceassociated fauna during winter, when ice cover is at a maximum and primary production in the water column as well as zooplankton standing stock at the surface is at a minimum (Hopkins and Torres, 1989; Schnack-Schiel etal., 1991). As in C.acutus, dry weights and lipid levels of the various stages of C.propinquus were generally lower in late winter/early spring as compared to the summer and autumn data. In C.acutus, lipid levels in winter consistently increased towards older stages, whereas in C.propinquus these decreased again in the adults. We observed lipid-rich and lipid-poor specimens, particularly CV stages, at the same stations during late winter (500-0 m) (Hagen et al., 1993; Kattner et al., 1994). These may have had different developmental histories with the specimens poor in lipid having recently moulted. Since C.propinquus was actively feeding during winter, one explanation for the seasonal decrease in weight and lipid level may be somewhat poorer feeding conditions with respect to the phytoplankton during winter/spring, prior to the onset of primary production in the pelagial [Huntley, in Bathmann et al. (1993)]. During summer, CV stages and females rapidly accumulated lipids, mainly triacylglycerols (Hagen et al., 1993), which comprised half of their dry weight and indicated the importance of these lipids as an energy reserve for C.propinquus (Hagen, 1988). In the females, gonad formation and egg production in late winter/spring could be fuelled by energy from these internal resources prior to the start of primary production, which may account for the lipid decrease in the females similar to C.acutus. Rhincalanus gigas Little seems to be known for certain about the general life history of R.gigas. Our data show an ontogenetic migration pattern which has also been reported by Ommanney (1936). In autumn, the youngest copepodite stages occupied the surface layer, whereas the older stages stayed deeper, as also described by Zmijewska (1988) from the Antarctic Peninsula area. Males were found during 1560

19 Life cycle strategies of calanoid copepods all sampling periods in the eastern Weddell Sea, although in highest numbers in mid-november, at the end of January and in mid-april. The decrease in abundance of CIV and CV stages, and the increase in CII and CIII stages, at the end of January suggest that reproduction took place in November/December. Atkinson (1991) found that egg laying of R.gigas was a protracted process with peak activities prior to December and again later in the season. Zmijewska (1987) encountered nauplii of R.gigas in surface layers of the Bransfield Strait at the end of December and beginning of January. In eastern Weddell Sea surface waters, nauplii occurred in April and autumn spawning was also described by Marin (1988), Atkinson (1991), and Marin and Schnack-Schiel (1993). In winter, all stages except for nauplii and CI were present in the Scotia Sea (Atkinson, 1991). In September/October, Vladimirskaya (1979) collected stages CIII-CVI, but only a few CII, in the Scotia Sea/northern Weddell Sea, the same age structure as found in the eastern Weddell Sea. During winter, food sources other than phytoplankton may be utilized, since Arashkevich [(1978), in Bathmann et al. (1993)] reported opportunistic feeding of R.gigas on zooplankton and detritus. Based on the deviating lipid compositions as compared to C.acutus, Graeve et al. (1994) also suggested that R.gigas is not purely herbivorous. In March, Hopkins (1985b) found only a few R.gigas with food in their guts in the Antarctic Peninsula region, but at the same time of year Hopkins and Torres (1989) described R.gigas as actively feeding on phytoplankton and protozoans in the northwestern Weddell Sea. In May, near the Antarctic Peninsula, ~90% of the R.gigas surface population had food in their guts (Marin and Schnack-Schiel, 1993), whereas in winter (June-August) in the Scotia Sea R.gigas was trophically inactive (Hopkins et al., 1993). Owing to these inconsistent results, a 1- or 2-year life cycle is discussed for R.gigas (Marin, 1988; Atkinson, 1991; Bathmann et al., 1993). A seasonal pattern in dry weight and lipid content also emerged for R.gigas, with lower values during late winter/early spring and higher values during the summer and autumn period. Lipid levels were generally lower than in the other two species and never reached the value of 69%DW reported for R.gigas by Lee and Hirota (1973) from sub-antarctic waters. Apart from the hypothesis that R.gigas is suffering from the more extreme conditions in these southernmost regions of its area of distribution, other possible explanations for these moderate energy reserves in the Weddell Sea are recent moulting or insufficient food supply during winter (if there is no resting stage). In the females, a depletion in lipid reserves, mainly wax esters (Hagen, 1988), may also be caused by reproductive processes like gonad formation. Metridia gerlachei In mid-october, the bulk of M.gerlachei were concentrated below 500 m. In mid-november, the species was widely dispersed throughout the water column, but in summer and autumn more than two-thirds of the population were confined to the m layer. In contrast to the other three species, M.gerlachei was never encountered in maximum numbers at the surface, 1561

20 S.B.Schnack-Schiel and W.Hagen although in mid-february and April 15% of the population occurred in the upper 50 m. In the vicinity of South Georgia, Atkinson and Peck (1988) could not detect a seasonal migration for M.gerlachei. The species is usually described as a typical midwater copepod (e.g. Vervoort, 1965; Schnack et al., 1985; Boysen-Ennen and Piatkowski, 1988; Hopkins and Torres, 1988; Huntley and Escritor, 1992). Vervoort (1965) suggested that M.gerlachei starts to reproduce at the end of the austral summer. However, the occurrence of large numbers of early copepodids in December/January reported by Zmijewska (1987) and Huntley and Escritor (1992) indicates that the onset of spawning takes place much earlier in spring. Spawning may continue from November to January in the Antarctic Peninsula area (Huntley and Escritor, 1992). In the eastern Weddell Sea, Fransz (1988) found eggs and nauplii in October, and the presence of CI in our samples from October suggests the onset Of spawning in August/September. On the other hand, the occurrence of CI until May shows an extended spawning season. Hopkins (1985b, 1987) identified mainly diatoms, dinoflagellates, protozoans and occasionally metazoans in the guts of M.gerlachei. Diet diversity was higher in females as compared to late copepodite stages, whereas the guts of males contained only diatoms (Hopkins, 1987). Similar to C.propinquus, M.gerlachei specimens from the pack-ice region had a significantly greater zooplankton component to their diet, mainly the cyclopoid Oithona similis, as compared to open-water specimens. Feeding experiments during October/November in the southeastern Weddell Sea showed that in contrast to C.acutus and C.propinquus, CV stages and females of M.gerlachei fed at low rates on naturally occurring low food concentrations of <1 jig chlorophyll a I" 1. On the other hand, feeding rates similar to C.acutus and C.propinquus were observed with chlorophyll concentrations >10 u,g I" 1 (Schnack-Schiel, 1987). Dry weight and lipid data are scarce for M.gerlachei (Reinhardt and Van Vleet, 1986; Hagen, 1988; Donnelly et al., 1994). Our seasonal data on lipid accumulation indicate a steady increase in the females from late winter/spring and summer to autumn. The doubling of lipid levels in the CV stages from summer to autumn is even more remarkable. This species stays active during winter (Hopkins et al., 1993) and has an opportunistic feeding behaviour (Hopkins, 1985b, 1987; Huntley and Escritor, 1992;' Graeve et al., 1994). Although M.gerlachei does not rely on lipid reserves as much as C.acutus and C.propinquus, its more or less moderate lipid reserves may help overcome the reduced food supply during winter. These energy depots may also allow early gonad maturation and reproduction prior to the onset of phytoplankton production in spring. In conclusion, C.acutus, C.propinquus, R.gigas and M.gerlachei undergo seasonal vertical migrations in the eastern Weddell Sea: all species show a continuous upward migration from mid-october to mid-november and from the end of January to mid-february. They descend again into deeper water layers from mid-april to the beginning of May. On the other hand, their life cycle strategies differ strongly with respect to distribution, time of reproduction, and hence age structure, migration pattern and lipid reserves. In Table I, we have 1562

21 1. a 2. S. o 5.* s Table I. Summmary of life history data of four copepod species examined in the Weddell Sea Approximate size (mm) (females) Maximum dry weight ( xg) (females) Median abundance (no. m" 1 ) Seasonal migrations summer/late winter Feeding mode Overwintering stage Reproduction period Lipid content Major storage lipid C.acutus m/ m herbivorous no winter feeding CIV-CVI diapause spring-summer high wax esters C.propinqtius m/ m herbivorous-omnivorous active winter feeding CIII-CV no diapause early spring summer high triacylglycerols R.gigas m/ m herbivorous-omnivorous active winter feeding? CI1-CVI diapause? spring/autumn moderate wax esters M.gerlachei nloaded from at Alfred-Wegener-Institut fuer Polar- und Meeresforschung - Bibliothek on December 18, m/ m omnivorous active winter feeding C1I-CIII no diapause late winter-late summer moderate wax esters/triacylglycerols ON

22 S.B.Schnack-Schiel and W.Hagen summarized the important information on the life cycles of these dominant species. However, many questions on their life history (e.g. life cycle duration, reproduction, feeding behaviour, overwintering strategies, lipid budget) are far from resolved. More detailed investigations are necessary, especially during the dark seasons, as well as field studies in combination with physiological and biochemical measurements. Acknowledgements We are grateful to the captains and crews of RV 'Polarstern' for their support. Special thanks are due to Elke Mizdalski for sorting the samples. This is contribution no. 705 of the Alfred-Wegener-Institut. References Andrews,K.J.H. (1966) The distribution and life-history of Calanoides acutus (Giesbrecht). Discovery Rep., 34, Atkinson,A. (1991) Life cycles of Calanoides acutus, Calanus simillimus and Rhincatanus gigas (Copepoda: Calanoida) within the Scotia Sea. Mar. Biol., 109, Atkinson.A. and Peck.J.M. (1988) A summer-winter comparison of zooplankton in the oceanic area around South Georgia. Polar Biol., 8, Bathmann.U.V., Makarov.R.R., Spiridonov.V.A. and Rohardt.G. (1993) Winter distribution and overwintering strategies of common Antarctic copepod species (Crustacea, Calanoida) in the Weddell Sea. Polar Biol., 13, Boysen-Ennen,E. and Piatkowski.U. (1988) Meso- and macrozooplankton communities in the Weddell Sea, Antarctica. Polar Biol., 9, Boysen-Ennen.E., Hagen.W., Hubold.G. and Piatkowski.U. (1991) Zooplankton biomass in the ice-covered Weddell Sea, Antarctica. Mar. Biol., Ill, Chojnacki.J. and Weglenska.T. (1984) Periodicity of composition, abundance, and vertical distribution of summer zooplankton (1977/78) in Ezcurra Inlet, Admiralty Bay (King George Island, South Shetland). J. Plankton Res., 6, Donnelly.J., Torres.J.J., Hopkins.T.L. and Lancraft.T.M. (1994) Chemical composition of Antarctic zooplankton during austral fall and winter. Polar Biol., 14, Drits.A.V., Pasternak,A.F. and Kosobokova.K.N. (1993) Feeding, metabolism and body composition of the Antarctic copepod Calanus propinquus Brady with special reference to its life cycle. Polar Biol., 13, Folch.J., Lees.M. and Sloane-Stanley.G.H. (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem., 226, Fransz.H.G. (1988) Vernal abundance, structure and development of epipelagic copepod populations of the eastern Weddell Sea (Antarctica). Polar Biol., 9, Gatten.R.R., Sargent.J.R., Forsberg.T.E.V., O'Hara.S.C.N. and Corner,E.D.S. (1980) On the nutrition of zooplankton. XIV. Utilization of plankton by Calanus helgolandicus during maturation and reproduction. J. Mar. Biol. Assoc. UK, 60, Gieskes.W.W.C, Veth.C, Wohrmann.A. and Grafe.M. (1987) Secchi disc depth visibility world record shattered. Eos, 68, 123. Graeve.M., Hagen.W. and Kattner.G. (1994) Herbivorous or omnivorous? On the significance of lipid compositions as trophic markers in Antarctic copepods. Deep-Sea Res., 44, Hagen.W. (1988) On the significance of lipids in Antarctic zooplankton. Ber. Polarforsch., 49, (in German) [English version (1989): Can. Transl. Fish. Aquat. Scl, 5458, 1-149]. Hagen.W., Kattner.G. and Graeve.M. (1993) Calanoides acutus and Calanus propinquus, Antarctic copepods with different lipid storage modes via wax esters or triacylglycerols. Mar. Ecol. Prog. Ser., 97, Hirche.H.J. and Kattner.G. (1993) Egg production and lipid content of Calanus glacialis in spring: indication of a food-dependent and food-independent reproductive mode. Mar. Biol., 117, Hopkins.T.L. (1985a) The zooplankton community of Croker Passage, Antarctic Peninsula. Polar Biol., 4,

23 Life cycle strategies of calanoid copepods Hopkins.T.L. (1985b) Food web of an Antarctic midwater ecosystem. Mar. Biol., 89, Hopkins.T.L. (1987) Midwater food web in McMurdo Sound, Ross Sea, Antarctica. Mar. Biol., 96, Hopkins.T.L. and Torres.J.J. (1988) The zooplankton community in the vicinity of the ice edge, western Weddell Sea, March Polar Biol., 9, Hopkins.T.L. andtorres,j.j. (1989) Midwater food web in the vicinity of a marginal ice zone in the western Weddell Sea. Deep-Sea Res., 36, Hopkins.T.L., Lancraft.T.M., Torres.J.J. and Donnelly,J. (1993) Community structure and trophic ecology of zooplankton in the Scotia Sea marginal ice zone winter. Deep-Sea Res., 40, Hubold.G. and Hempel.I. (1987) Seasonal variability in the southern Weddell Sea. Meeresforschung 31, Huntley.M. and Escritor.F. (1991) Dynamics of Calanoides acutus (Copepoda: Calanoida) in Antarctic coastal waters. Deep-Sea Res., 38, Huntley.M. and Escritor.F. (1992) Ecology of Metridia gerlachei Giesbrecht in the western Bransfield Strait, Antarctica. Deep-Sea Res., 39, Kattner.G., Graeve.M. and Hagen.W. (1994) Ontogenetic and seasonal changes in lipid and fatty acid/alcohol compositions of the dominant Antarctic copepods Calamus propinquus, Calanoides acutus and Rhincalanus gigas. Mar. Biol., 118, Lee.R.F. and Hirota.J. (1973) Wax esters in tropical zooplankton and nekton and the geographical distribution of wax esters in marine copepods. Limnol. Oceanogr., 18, Marin.V. (1987) The oceanographic structure of the eastern Scotia Sea IV. Distribution of copepod species in relation to hydrography in Deep-Sea Res., 34, Marin.V. (1988) Qualitative models of the life cycles of Calanoides acutus, Calanus propinquus and Rhincalanus gigas. Polar Biol., 8, Marin.V.H. and Schnack-Schiel.S.B. (1993) The occurrence of Rhincalanus gigas, Calanoides acutus and Calanus propinquus (Copepoda: Calanoida) in late May in the area of the Antarctic Peninsula. Polar Biol., 12, N6thig.E.-M., von Bodungen.B. and Sui.O. (1991) Phyto- and protozooplankton biomass during austral summer in surface waters of the Weddell Sea and vicinity. Polar Biol., 11, Ommanney.F.D. (1936) Rhincalanus gigas (Brady) a copepod of the southern macroplankton. Discovery Rep., 13, Ottestad.P. (1932) On the biology of some southern copepods. Hvalr&dets Skr., 5, Ottestad.P. (1936) On Antarctic copepods from the 'Norvegia' Expedition Scientific Results of the Norwegian Antarctic Expeditions el SQQ 15, pp Reinhardt.S.B. and Van Vleet.E.S. (1986) Lipid composition of twenty-two species of Antarctic midwater zooplankton and fish. Mar. Biol., 91, Scharek.R. (1991) Die Entwicklung des Phytoplanktons im ostlichen Weddellmeer(Antarktis) beim Obergang vom Spatwinter zum Fruhjahr. Ber. Polarforsch., 94, Schnack-Schiel.S.B. (1987) Die Winter-Expedition mit FS 'Polarstern' in die Antarktis (ANT V/l- 3). Ber. Polarforsch., 39, Schnack.S.B., Marschall.S. and Mizdalski.E. (1985) On the distribution of copepods and larvae of Euphausia superba in Antarctic waters during February Meeresforschung, Schnack-Schiel.S.B., Hagen.W. and Mizdalski.E. (1991) A seasonal comparison of Calanoides acutus and Calanus propinquus (Copepoda: Calanoida) in the southeastern Weddell Sea, Antarctica. Mar. Ecol. Prog. Ser., 70, Spindler.M., Dieckmann.G. and Thomas,D. (1993) Die Expedition Antarktis X/3 mit FS 'Polarstern" Ber. Polarforsch., 121, Vervoort.W. (1965) Notes on the biogeography and ecology of free-living marine Copepoda. In v. Miegham.J. and v. Oye.P. (eds), Biogeography and Ecology in Antarctica. Dr W.Junk Publishers, The Hague, Vol. XI, pp Vladimirskaya.Ye.V. (1979) Winter distribution of mass species of copepods in the southern part of Scotia Sea. Oceanology, 18, Voronina.N.M. (1970) Seasonal cycles of some common Antarctic copepod species. In Holdgate. M.V. (ed.), Antarctic Ecology. Academic Press, London, Vol. 1, pp Voronina.N.M. (1978) Variability of ecosystems. In Charnock.H. and Deacon,G.E R. (eds). Advances in Oceanography. Plenum Press, New York, pp Zmijewska.M.I. (1983) Copepoda (Calanoida) from the Prydz Bay (Antarctica, Indian Ocean Sector). Pol. Polar Res., 4, Zmijewska.M.I. (1985) Copepoda in the southern part of Drake Passage and in Bransfield Strait during early summer (BIOMASS-SIBEX, December-January). Pol. Polar Res., 6,