The reproductive cycle and life history of the Arctic copepod. Calanus glacialis in the White Sea. Accepted: 27 April 1999. Abstract Seasonal variations in the ...
Polar Biol (1999) 22: 254±263
Ó Springer-Verlag 1999
ORIGINAL PAPER
K.N. Kosobokova
The reproductive cycle and life history of the Arctic copepod Calanus glacialis in the White Sea
Accepted: 27 April 1999
Abstract Seasonal variations in the gonad development and sex ratio of copepodite stage V (CV) and adults were examined from February to November in order to understand the reproductive cycle and the life history of Calanus glacialis in the White Sea. Gonad maturation, sexual dierentiation and moulting to adults take place during the 2nd year of development. Energy accumulation takes place in the spring and summer of the 2nd year. The following autumn/winter is the major period of CV maturation, which occurs independent of food supply. Maturation of males precedes that of females by 2± 3 months. The maximum proportions of CV and adult males are found in the population in October and November. The onset of female maturation is observed in February and March, ca. 2 months prior to the spring phytoplankton bloom. Reproduction takes place between April and June. Its termination in the second half of June coincides with the warming of the surface water layer where egg laying takes place. Variations in the gonad morphology throughout the year suggest long life spans and iteroparity of females of C. glacialis in the White Sea. Many of them survive for several months after reproduction and are able to overwinter again. Therefore, females with dierent life histories co-occur in the population in winter: ``young'' females recently moulted from the overwintering CVs, and ``old'' females which have spawned at least once in their life, after which they return to overwintering conditions. In contrast, males have shorter life spans of 3±4 months resulting in a sex ratio skewed toward females at all seasons.
Introduction The Arctic calanoid copepod Calanus glacialis Jaschnov is one of the dominant species in the plankton K.N. Kosobokova P.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, 36 Nakhimov Ave., 117218 Moscow, Russia
communities of the Arctic Basin, its peripheral seas, and the adjacent areas of the Atlantic and Paci®c Oceans. The distribution of C. glacialis is related to the distribution of the Arctic water masses in the northern hemisphere (Jaschnov 1970; Conover 1988). In the Atlantic Ocean this species is found as far south as Nova Scotia (Runge et al. 1985), and in the Paci®c in the northern part of the Sea of Okhotsk (Jaschnov 1955). In the White Sea C. glacialis is one of the major components of zooplankton, accounting for 30±45% of its total biomass (Pertzova 1971). This Arctic sea was formed during the last interglacial period and had subsequently lost its direct connection with the Arctic region as a result of the warming of the climate and the penetration of the warm North Cape Current into the southern part of the Barents Sea. Thus, the White Sea population of C. glacialis is a relict of the glacial period, isolated at present from populations inhabiting the largest part of its distribution area. The closely related boreal species C. ®nmarchicus seldom occurs in the White Sea. It does not reproduce there and has never been found there in numbers (Jaschnov 1966; Kosobokova and Pertzova 1990). The estimated duration of the life cycle of C. glacialis in the dierent parts of its area is still under dispute (Tande 1989; Smith and Schnack-Schiel 1990). The life cycle is generally thought to be biennial north of the polar front and annual over the rest of the area (Conover 1988). In the northern Barents Sea and the Arctic Ocean generation time is apparently 2 years, with CIV being the main overwintering stage (Pavshtiks 1977; Kosobokova 1981, 1986; Tande et al. 1985). A 1-year cycle has been suggested for the Greenland Sea (Smith 1990), Davis Strait (Huntley et al. 1983) and the Sea of Okhotsk (Safronov 1984). In some areas C. glacialis demonstrates equivocal characteristics suggesting a combination of an annual and biennial cycle (Grainger 1963; Maclellan 1967; Melle and Skjoldal 1998), which probably represents survival of early and late cohorts (Hirche 1989). In the White Sea the life cycle of C. glacialis is considered to be biennial, with spawning in
255
May and June, and CIV dominating the overwintering stock (Prygunkova 1968; Kosobokova and Pertzova 1990). The major confusion concerning the length of the C. glacialis life cycle is related to the simultaneous presence of young and late developmental stages during the summer months (Tande et al. 1985; Hirche 1989), and almost year-round presence of CV and adult females in some areas (Kosobokova and Pertzova 1990). In this situation, the data on developmental stage composition hardly allow the distinction to be made between new and overwintered generations, in order to estimate the life spans of CV and adults, and to assess the full length of the life cycle. The experimental evidences that C. glacialis females are long living and lay eggs for 10 months when fed (Hirche 1989; Kosobokova 1990) further complicate understanding of the life cycle. Observations of copepod gonad maturation have often been used for life-cycle studies, as the method for interpretation of development in the late phases of the life history (Tande and Hopkins 1981; Tande and Gronvik 1983; Norrbin 1991). In this study we examined the gonad morphology of C. glacialis copepodite stage V and adults in the White Sea throughout the entire annual cycle in order to reconstruct the cycle of gonad development and to ®ll gaps in understanding of the life cycle. The present study aimed: (1) to estimate the season of the CV sexual dierentiation and timing of moulting to adults; (2) to determine the timing and duration of the reproductive period; (3) to follow the fate of adult females after reproduction; (4) to assess the life spans of CV, adult males and females in the wild. Study area The White Sea adjoins the Barents Sea to the southwest of the Kola Peninsula (Fig. 1). The sea is usually covered with ice for 5±7 months, from November to May (Timonov 1950). The winter temperature of the upper layer is close to the freezing point. After the ice break-up in May, temperature gradually rises from )1.7°C to 4± 6°C by the end of June. Summer temperatures (July/ August) near the surface usually reach 12±14°C, occasionally rising to 25°C. The water mass below 50 m maintains a negative temperature, and salinity remains constant at 29.7 throughout the year (Timonov 1950). Melting of snow and ice in April/May is accompanied by phytoplankton growth at the ice-water interface (Fedorov and Bobrov 1977). The spring diatom bloom takes place in mid-May just after the ice break-up (Kokin and Koltzova 1972). Highest concentrations of phytoplankton and maximum primary production are recorded in the upper 0- to 25-m water layer (Fedorov and Bobrov 1977). In June, nutrient depletion and zooplankton grazing result in a rapid decrease of the phytoplankton concentration in the uppermost water layer. In July, a summer diatom bloom formed by the large diatoms Skeletonema costatum and Coscinodiscus
Fig. 1 Station locations in the Kandalaksha Bay and the basin of the White Sea. A and B show positions of two permanent stations with depths of 105 and 15 m, respectively
asteromphalus (Beklemishev et al. 1975) is observed in the subsurface layer with maximum biomass below 25 m depth. At the end of August dino¯agellates demonstrate a slight increase (Fedorov and Bobrov 1977). In September/October very low concentrations of phytoplankton and low primary production indicate the termination of the productive season (Fedorov and Bobrov 1977).
Materials and methods Multi-year zooplankton collections of the White Sea Biological Station (WSBS) of Moscow State University were used for the present study. Zooplankton was collected between 1972 and 1991 in the Kandalaksha Bay and in the basin of the White Sea (Fig. 1). Sampling was carried out with a closing Juday net (mouth opening 0.1 m2, mesh size 180 lm). Samples were preserved in 4% boraxbuered formalin. Samples for the study of the stage composition of the Calanus glacialis population were collected at a permanent station in Kandalaksha Bay (station A, depth 105 m, Fig. 1). Sampling was carried out from February to November 1976, once or twice per month (Table 1). Sampling layers were 0±10, 10±25, 25±50 and 50± 100 m. In February, March and April, when the sea was covered with ice, zooplankton was collected through a hole in the ice. In May, when station A was inaccessible either by ship or from the ice due to ice break-up, samples were collected from a row-boat at permanent station B (depth 15 m), close to the WSBS (Fig. 1). The same collections (Table 1) were used to examine gonad maturation in CV and adults. In addition, samples from several stations in the Kandalaksha Bay and the White Sea Basin (depths 50±280 m) were used (Table 2). Samples of dierent years were examined in order to reconstruct the entire annual cycle of gonad development, and to assess interannual variability. From 3 to 27 samples were analysed for each month of the calendar year (Table 2). From 20 to 100 individuals of CV and adult females from each sample were stained in a borax carmine solution according to Tande and Hopkins (1981) and examined under a stereomicroscope. The size of oocytes was measured in diverticulae and
256 Table 1 List of zooplankton samples collected in 1976 in Kandalaksha Bay of the White Sea and used in the present study for analysis of the population dynamics in Calanus glacialis
Date
Station
Depth (m)
Sampling layers
07±09 Feb 16 Mar 15±16 Apr 4 Jun 21±22 Jun 6 Jul 26±27 Jul 6 Aug 17±18 Aug 10±11 Sep 20±21 Oct 21±22 Nov 2 Mar 5 Mar 4 Apr 11 Apr 25 Apr 4 May 10 May 15 May
A A A A A A A A A A A A B B B B B B B B
105 105 105 105 105 105 105 105 105 105 105 105 15 15 15 15 15 15 15 15
0±10, 0±10, 0±10, 0±10, 0±10, 0±10, 0±10, 0±10, 0±10, 0±10, 0±10, 0±10, 0±15 0±10 0±15 0±15 0±15 0±15 0±15 0±15
oviducts inside intact females under a light microscope at a magni®cation 7 ´ 20 ´ 1.5. When oocytes formed several rows, the diameter of the largest oocytes (most mature, according to Nieho 1998) in the ventral row inside the diverticulae and oviducts was measured. The length-frequency distribution of CV and adults was examined in June, October and November 1991. Between 100 and 200 individuals from each sample were measured from the tip of the cephalosome to the distal lateral end of the last thoracic segment.
Results Developmental stage composition Seasonal variations of the abundance and developmental stage composition of the Calanus glacialis population at stations A and B in Kandalaksha Bay in 1976 are shown in Fig. 2. It is convenient to take May and June as a starting point, since major spawning takes place in the upper 0- to 25-m water layer during these months, according to the occurrence of eggs and nauplii. Copepodite stage I (CI) was present from May until the end of June. Growth and development of the young stages (nauplii and CI±CIII) took place in the surface layer 0± 25 m. By August there was a new generation of mostly CIV (Fig. 2), which then descended below 50 m into the colder deep water. Beginning in August, the proportion of CV did not show any remarkable increase thus indicating that further development of new recruits had been arrested. CIV clearly dominated the population in early autumn. CIII was the youngest developmental stage present in a very low proportion (about 1%), while CV and CVI contributed about 40% (Fig. 2). In winter (from February to April) the population consisted of CIII (a few), CIV, CV, adult females and males (Fig. 2). A higher proportion of adults in February and March compared to April seemed to be a
10±25, 10±25, 10±25, 10±25, 10±25, 10±25, 10±25, 10±25, 10±25, 10±25, 10±25, 10±25,
25±50, 25±50, 25±50, 25±50, 25±50, 25±50, 25±50, 25±50, 25±50, 25±50, 25±50, 25±50,
Number of samples 50±100 50±100 50±100 50±100 50±100 50±100 50±100 50±100 50±100 50±100 50±100 50±100
8 4 8 4 8 4 8 4 8 8 8 8 1 1 1 1 1 2 1 1
consequence of sampling in the relatively shallow area. It has been shown previously that CIV of overwintering stock concentrates below 100 m in winter (Prygunkova 1974), while some adult females migrate to the upper layers in February and March and are spread over the shallow area by tidal currents (Prygunkova 1974; Kosobokova and Pertzova 1990). We suggest that these ascendant females were collected at station A in February and March during our observations while deeperliving CIV were poorly represented. In spring (May) the bulk of the overwintering stock represented by CIV, CV and adults (Fig. 2) migrated from the depths to the surface to continue growth and development. In late spring (June), a short (about 2 weeks) period was observed when CIV disappeared almost completely. The simultaneous increase of CV numbers suggested that this was a period of major moulting of overwintering CIV to CV. The increase of CV numbers was observed during the same period when nauplii of the new generation were at the peak concentration (Fig. 2). Gonad development and sex ratio in CV and adults Gonad development in Calanus glacialis starts at CIV. Sexual dierentiation takes place late during CV development, when potential males and females can be easily distinguished by the anatomy of their gonads (Tande and Hopkins 1981). To follow the development of CV derived after moulting from the overwintering CIV, the anatomy of CV gonads was examined starting in May/ June. All CVs in the present collections had sexually undierentiated immature gonads from the end of May until the end of July. Through this period the mean length of gonads increased from 75±100 to 200±400 lm. First individuals with a male-type reproductive system
257 Table 2 List of zooplankton samples collected in Kandalaksha Bay and the basin of the White Sea and used in the present study for investigation of gonad development in Calanus glacialis CV and females Date
07±09.02.76 01.03.86 07.03.86 16.03.76 18.03.86 31.03.76 03.04.76 10.04.76 21.04.76 04.05.76 28.05.91 03.06.91
06.06.87 08.06.73 09.06.80 12.06.72 16.06.87 17.06.87 26.06.91 28.06.86 29.06.91 02.07.72 03.07.72 03.07.72 03.07.72 04.07.72 08.07.72 09.07.72 27.07.91 06.08.76 09.08.73 11.08.73 12.08.73 13.08.73 15.08.90 21.08.87 24.08.90 15.09.83 16.09.83 06.10.76 10.10.87 15.10.76 16.10.91 24.10.91 21±22.11.76
No. station
A B B A B B B B B B 1 2 5 6 12 7 5 A A A A A A 4 78 4 5 10 11 12 14 30 31 4 A 5 78 83 85 3 3 3 A A A 1 A A 9 78 A
Depth (m)
105 15 15 105 15 15 15 15 15 15 60 120 250 100 200 50 250 105 105 105 105 105 105 220 270 220 283 138 258 205 217 190 255 220 105 220 270 125 200 200 200 200 105 105 105 60 105 105 200 255 105
Sampling layers (m)
0±10, 10±25, 25±50, 50±100 0±5 0±5 0±10, 10±25, 25±50, 50±100 0±5 0±5 0±15 0±15 0±15 0±15 0±bottom 0±bottom 0±bottom 0±5 0±5 0±bottom 0±bottom 0±10, 10±25, 25±50, 50±100 0±10, 10±25, 25±50, 50±100 0±10, 10±25, 25±50, 50±100, 0±100 0±50, 50±100 0±30, 30±60, 60±120 0±100 0±50, 50±100, 100±150, 150±214 0±250 0±50, 50±100, 100±211 0±50, 50±100, 100±200, 200±280 0±50, 50±100, 100±135 0±50, 50±100, 100±200, 200±255 0±50, 50±100, 100±200 0±50, 50±100, 100±200 0±50, 50±100, 100±187 0±50, 50±100, 100±200 50±219, 100±220 0±90 0±10, 10±25, 25±50, 50±100, 100±200 100±200, 200±286, 200±265 50±122 50±120, 100±196, 100±182 0±50, 50±185, 90±200 0±50, 50±150 0±50, 50±100, 85±200 0±110 0±110 0±50, 50±100 0±25, 25±bottom 0±50, 50±100 0±50, 50±100 0±200 0±250 0±10, 10±25, 25±50, 50±100
were found in the last days of July. At that time the proportion of males in the CV population was extremely low (0.6%). It increased from August to October, when it reached the maximum of 41% (Table 3). From February to July phenotypic CV males were not found. Seasonal variations in the sex ratio of adults were similar to those in CV (Table 3). Both in CV and adult Calanus glacialis, the sex ratio favoured females in all seasons. The maximum proportion of adult males was
Number of samples
Number of ind. examined Adults
CVs
8 2 1 4 2 1 1 1 1 1 1 1 1 1 1 1 1 4
66 58 107 42 21 7 2 1 4 3 7 104 58 209 7 6 147 19 7 37 5 1 0 5 186 28 14 4 5 6 10 4 7 217 4 21 58 15 89 104 61 41 19 0 0 0 11 0 68 57 37
6 1 2 7 2 0 0 0 0 0 27 74 32 215 27 102 0 3 3 110 38 79 82 35 0 31 0 87 73 43 0 0 0 2 18 24 66 18 105 165 0 165 53 6 66 4 10 21 46 42 14
5 2 3 1 4 1 3 4 3 4 3 3 3 3 4 1 5 4 1 3 3 2 3 1 1 2 2 4 2 1 1 8
observed in October, very close to the time of maximum CV males' occurrence, suggesting that maturation and moulting of CV males to adults took place soon after visible sex dierentiation. Moulting of CV to adult females seems to occur very seldom in the summer and autumn, as the proportion of young immature females (Fig. 3a) did not exceed 1±2% and 5±10% of the female population in these two seasons, respectively (Fig. 4). The maximum proportion of young adult females, about
258
Fig. 2 Abundance (ind/m3) and developmental stage composition of the Calanus glacialis population from February to November 1976 at permanent station A
40% of the female population, was found in the winter, i.e. February (Fig. 4). Gonad development in adult females A brief description of dierent stages of female maturity observed during the present study is presented in Table 4. Young immature females (stage 1) have a compact ovary of about 750 ´ 250 lm in size (Fig. 3a). They appear in numbers in winter and commence maturation from March (Fig. 4). The maturation is associated with the appearance of small oocytes (diameter about 40 lm) in diverticulae and oviducts (stage 2, Fig. 3b). The complete cycle of maturation takes about 2 months. The ®rst females in spawning condition (stage 4, mature, Fig. 3c), with the largest oocytes of 120± 160 lm and greatly enlarged ovary reaching the third thoracic segment, appear in the plankton at the end of April. Their proportion gradually increases until midMay when nearly all females reach maturity (Fig. 4). From mid-June the proportion of mature females goes down, while that of semi-spent females of the next stage
Fig. 3 Stages of gonad maturity in Calanus glacialis adult females: a young immature (stage 1), b semi-mature (stage 2), c mature (stage 4), d semi-spent (stage 5), e spent (stage 6), f rematuring (stage 7)
(5) (Fig. 3d) increases (Fig. 4), indicating termination of the reproductive period. Termination of spawning coincides with the summer warming of the upper water layer that forces females to migrate downward into layers with negative temperatures. At the beginning of July no indication of reproduction was observed at depths from a plankton survey of eggs and nauplii, despite the fact that some of the descended females still had oocytes in their ovaries. Within about 2 weeks after the descent, semi-spent females are replaced by females with empty gonads
Table 3 Seasonal variations of the sex ratio in Calanus glacialis CVs and adults Months
II
III
IV
V
VI
VII
VIII
IX
X
XI
CV, male : female Adults, male : female
0 0.17
0 0.03
0 0.02
0 0.0006
0 0.004±0.02
0.006 0.01
0.01±0.04 0.02±0.04
0.2 0.04
0.7 0.6
0.6 0.5
259
The potential males belong to the larger modal group, while potential females cover the whole size range (Fig. 5b). Table 4 Reproductive stages of Calanus glacialis adult females Stage Morphological description 1 2 3 4 Fig. 4 Seasonal variation of gonad maturity in Calanus glacialis adult females. See Table 3 for de®nition of reproductive stages
(stage 6, Fig. 3e). Non-released oocytes seem to undergo a rapid resorption. However, the microscopic examination showed that oogonia were still present in the posterior of the ovaries of spent females. These females were present in the population below 100 m from July until mid-winter (Fig. 4) when they still composed ca. 60% of the female population. Their ovaries did not undergo shrinkage and were as long as those of ripe females. The anatomy of the ovaries, as well as the lipid content and body transparence of spent females, diered considerably from those of young immature females present simultaneously and which composed other 40% of the female population in the winter (Fig. 4). The former had much larger oil sacs and were less transparent compared to the young females. Distinct dierences between these two groups of females, as well as the absence of any transitional forms between them, suggest co-occurrence of females with dierent life histories in the winter population of Calanus glacialis. In mid-February maturation of new oocytes was observed in the gonads of spent females. By that time their long ovaries had became ®lled with small oocytes with a diameter of 30± 40 lm. Two or three rows of immature oocytes of the same size were present also in the diverticula and oviducts (Fig. 3f ). This stage of gonad maturity is found in Calanus for the ®rst time and is classi®ed here as a ``stage 7, rematuring'' (Table 4).
5 6 7
Immature (young); ovary compact, no oocytes in diverticulae and oviducts Semi-mature a; anterior ends of diverticulae widely separated, diverticulae with single row of small oocytes; single row of small oocytes in oviducts Semi-mature b; diverticulae with several rows of small oocytes; more than one row of oocytes in oviducts Mature; diverticulae close together, ®lled with several rows of large oocytes; pouches of large oocytes in oviducts Semi-spent; few large oocytes in the ovary, diverticulae and oviducts with single irregularly spread oocytes Spent; diverticulae and oviducts thin bands; no oocytes in the ovary, posterior of ovary extends to the third thoracic segment Rematuring; large ovary ®lled with small oocytes extends to the third thoracic segment; anterior ends of diverticulae widely separated, diverticulae and oviducts with one or two rows of small oocytes
Length-frequency distribution in CV and adults Figure 5 demonstrates the length-frequency distribution of the prosome length of CV in June, when sex has not yet been dierentiated, and in October/November, when dierences between potential males and females were well pronounced. The length-frequency histogram is clearly polymodal in June (Fig. 5a). In October/ November, CV males and females form two modal groups with substantially dierent means. The dierence is statistically signi®cant (Student's t-test, P < 0.001).
Fig. 5 Length-frequency diagrams of Calanus glacialis CV and adults. A Length-frequency distribution of CV in early summer (June). B Same in autumn (combined data for October and November). C Length-frequency distribution of adults (combined data for October and November)
260
The length-frequency distribution of adults shows a reverse picture (Fig. 5c). Females and males form two discrete size groups, and adult males belong to the smaller modal group of adults. There is almost no overlap of size ranges of males and females. It is worth noting that the mean prosome length of adult males shows a very slight increase compared to the CV males (the dierence is statistically signi®cant: Student's t-test, P < 0.001). By contrast, the size of adult females is signi®cantly larger (Student's t-test, P < 0.001) compared to both CV females and adult males (Fig. 5b,c).
Discussion The 2-year life cycle of Calanus glacialis in the White Sea was proposed by Prygunkova (1968) based on a 6-year investigation of stage distribution at an inshore site with depth of 60 m. According to her study, a major evidence for the 2 year cycle is an annual maximum of CV in spring (May), observed every year prior to an annual maximum of nauplii and CI of a new generation. This CV maximum was observed almost simultaneously with the decrease of the CIV abundance which had been taken as an indication of moulting of overwintering CIV to CV (Prygunkova 1968). Sex dierentiation and maturation of adults have been suggested to occur in winter as most males were found between October and April. However, data for the winter period in this study were very poor, as the Calanus glacialis population was almost absent at the studied site from October to May due to the seasonal descent to greater depths (Prygunkova 1968). Most suggestions concerning timing of moulting and maturation of CV and adults (Prygunkova 1968, 1974) have not been substantially supported by ®eld observations. Later observations by Kosobokova and Pertzova (1990), undertaken in the open sea at locations with depths of 100±300 m con®rmed that the Calanus glacialis overwintering population consists of CIV±CVI and concentrates in the deepest part of Kandalaksha Bay from October to April. The present data on the population dynamics of Calanus glacialis strongly con®rm earlier observations (Prygunkova 1968, 1974; Kosobokova and Pertzova 1990). The stage distribution shows that the spring spawning of Calanus in May/June produces recruits that develop to CIV by August and enter diapause. The
gonad maturation clearly indicates that they continue to CV during the spring/summer the following year, then mature in the autumn/winter and, ®nally, spawn at the age of 2 years (Fig. 6). Thus, it takes 2 years for the majority of the stock to mature in the White Sea. The development of the overwintering stock takes place along with the growth and development of a new generation (Fig. 6). During spring and summer of the 2nd year, energy is actively accumulated, as has been shown by the seasonal study of the Calanus glacialis lipid content (Kosobokova 1990). The spring moulting of overwintering CIV to CV is followed by a four- to sixfold increase of the lipid content (Kosobokova 1990). Lipid accumulation during the summer results in a 1.5to twofold increase of the CV lipids (Kosobokova 1990). In May/June, lipid accumulation takes place in the upper water layers. However, at the end of June warming of the upper layer forces late developmental stages to leave for depths below 50 m (Kosobokova and Pertzova 1990). The source of food for further lipid accumulation is not completely clear, although CVs and females with food in their guts are found regularly below 50 m depth (Kosobokova and Pertzova 1990). In July, descended copepods apparently use the sinking diatom bloom (Beklemishev et al. 1975). In August they may feed close to the surface at night during diel vertical migration (Kosobokova and Pertzova 1990). The lipid accumulation in CVs is accompanied by enlarging of their gonads during the summer. The commencement of sexual dierentiation becomes evident by the end of the summer when the ®rst CV individuals with a male-type gonad appear (Table 3). The seasonal pattern of maturation is similar to that previously described for the closely related species Calanus ®nmarchicus in Norwegian fjords (Tande and Hopkins 1981). In both species male dierentiation is timed to autumn/winter and is followed almost immediate by moulting to adult males. Maturity of males is attained simultaneously with the ®nal moult (Grigg and Bardwell 1982; Grigg et al. 1985). The moulting of CV males to adults precedes that of CV females by 2±3 months. Female maturation in both species starts in winter irrespective of the onset of the phytoplankton bloom. In Calanus glacialis it takes 2±3 months, from February/ March to April/May. Fig. 6 Scheme of the Calanus glacialis life cycle in the White Sea. Asterisks indicate egg-laying period
261
Sex dierentiation, maturation of males and early stages of female maturation in Calanus species apparently depend on internal energy resources (Tande and Hopkins 1981; Hirche and Kattner 1993; Nieho and Hirche 1996), as they take place when there is no phytoplankton in the sea. Maturation and further survival of males is assumed to depend completely on stored lipids, as they are mostly present during the unproductive season (Table 3). Similar to Calanus ®nmarchicus, Calanus glacialis males derive from the largest size fraction of CV (Fig. 5a) (Grigg et al. 1981, 1985; Miller et al. 1991). Metabolism associated with male maturation appears to be so energy demanding that body length of Calanus glacialis males increases only when moulting from CV (Fig. 5b,c). This is not surprising as spermatozoa contain relatively more proteinaceous substances than ova, and protein synthesis consumes more energy than any other biosynthetic process (Lehninger 1975). Thus, the male tactics in Calanus glacialis are not to spend energy for somatic growth but rather keep it for fuelling the maturation process, searching for females and mating. Most of them disappear by the onset of the phytoplankton bloom, as high energy demands in the absence of food result in a short life span (Table 3). Shorter life spans and less good feeding of males compared to females have been reported for several calanid species (Vervoort 1951; Marshall and Orr 1955; Norrbin 1993, 1994). The limited seasonal occurrence and short life spans of the Calanus glacialis males support a general conclusion that male calanids have only a shortlived function and once that is achieved, they are expendable (Conover 1988). The maturation of the female gonad takes much longer compared to that of the male. In Calanus glacialis, the female gonad passes through several stages, which can be easily distinguished by microscopic examination. Several classi®cation schemes have been reported for the assessment of maturity in calanoids (Marshall and Orr 1955; Runge 1987; Smith 1990; Smith and Lane 1991; Tourangeau and Runge 1991; Kosobokova 1994; Nieho and Hirche 1996; Spiridonov and Kosobokova 1997). Most of these were based on observations made during the spawning period and were aimed at the assessment of the activity of reproduction under dierent environmental conditions (Smith 1990; Tourangeau and Runge 1991; Hirche et al. 1994; Schnack-Schiel and Hagen 1995; Nieho and Hirche 1996). Maturity stages of Calanus glacialis found during the present study in the spring and summer are in good agreement with those previously described for Calanus. The seasonal variations in the proportion of the dierent stages allow one to estimate the timing of the commencement of reproduction and duration of the reproductive period. The high proportion of mature females (stage 4) shows that Calanus glacialis may commence reproduction in the White Sea in April (Fig. 4), before the ice break-up. Egg laying seems to be at its peak in May, lasting until early July. A comparison between years diering in thermal regime suggests that termina-
tion of reproduction could be linked to the seasonal warming of the surface water. In particular, in the years when the surface temperature during June did not dier greatly from the average annual values and reached +10°C by the end of the month, reproduction terminated by the end of June (Kosobokova 1993). In years with colder May and June, egg-laying has been observed until the ®rst week of July (Kosobokova 1993). Previous investigations indicated a considerable geographical variation in the timing of Calanus glacialis reproduction. In most cases reproduction was observed during the primary production period and was de®nitely coupled with the presence of phytoplankton (Maclellan 1967; Tande et al. 1985; Hirche and Bohrer 1987; Kosobokova 1993; Hirche and Kwasniewski 1997). At the same time, several observations suggested the possibility of Calanus glacialis recruitment at extremely low chlorophyll concentrations. Smith (1990) found spawning Calanus glacialis females in the marginal ice zone of the Greenland Sea around the beginning of April prior to phytoplankton growth. In the central Canadian Arctic, spawning was initiated under 2 m of seasonal ice in June in anticipation of the spring bloom (unpublished data by Conover and Harris in Conover 1988). Hirche and Kattner (1993) in the western Barents Sea proved experimentally that spawning of Calanus glacialis prior to pelagic phytoplankton growth does take place. They suggested that this is a regular part of its life cycle in the Arctic ice-covered seas, which allows it to exploit the patchy phytoplankton blooms in local openings and polynyas early in the year and gives certain advantages to the ospring in an unpredictable environment. Early reproduction of Calanus glacialis also seems possible in the White Sea as mature females are present in the population well before the ice break-up. However, as in most areas, the maximum proportion of mature females is observed during the phytoplankton bloom (Fig. 4) indicating a clear reproductive response of Calanus glacialis to food supply. The factors responsible for the termination of spawning in the ®eld have not been documented so far; however, laboratory experiments suggest that food deprivation is one of the most important factors (Hirche and Bohrer 1987; Hirche 1989). Our observations in the White Sea suggest that the water temperature could be another factor controlling the duration of the Calanus glacialis reproductive season in areas with a pronounced seasonal warming of the surface layer. The fate of copepod females after termination of spawning is poorly studied (Drits et al. 1993; Kosobokova 1993; Hagen and Schnack-Schiel 1996). Evidences that in large Calanus species females are longliving and able to reproduce a second time during their life have been discussed by Conover (1988) and Hirche and Nieho (1996). Conover and Sieferd (1993) suggested such iteroparity, i.e. the capability to spawn in two successive reproductive seasons, for Calanus hyperboreus. The capability of Calanus glacialis females to survive up to 9 months without feeding and to
262
conserve their reproductive capacity for at least 7 months has been demonstrated in laboratory experiments (Hirche 1989; Kosobokova 1990). The pre-collection history of these females was unknown and therefore it was not clear whether they had spawned before the experiment. The present observations on the states of the female gonads in the White Sea indicate that a large portion of the Calanus glacialis females that have participated in reproduction in spring do survive for more than 9 months after the end of the reproductive season. The non-spawned oocytes in their gonads undergo fast degradation just after ceasing of spawning, but the rest of the oogonia seem to give rise to new oocytes after one more overwintering. As a result, two types of females co-occur in late winter: ``old'' ones that have spawned at least once in their life and after that have undergone overwintering conditions, and ``young'' ones that have moulted from overwintering CV (Fig. 4). This observation is in good agreement with the suggestion by Hirche and Kattner (1993) that females with dierent life histories co-occur in areas with a 2-year life cycle. Most likely these two types of females have differing reproductive strategies. Speci®cally, maturation of the old females in the White Sea starts earlier (February) than that of the young ones (March), suggesting the earlier commencement of spawning. We speculate that the old females are the ones that could commence reproduction in anticipation of phytoplankton growth, relying on stored lipids, and demonstrating a food-independent reproductive mode as described by Hirche and Kattner (1993). The maturation of the lipid-poor young females is shifted to the later dates, suggesting later commencement of spawning, and apparently stronger dependence of egg laying on the food supply. Long life spans and iteroparity of females suggest also that some Calanus glacialis females in the White Sea are 3 or even 4 years old (Fig. 6). This, however, does not mean that Calanus has a 3- to 4-year life cycle in the study area, as development is completed and maturation is achieved for most of the stock within 2 years. The present data show that, similar to other calanids, adult males and females of Calanus glacialis have quite dierent life spans. While males survive for 3±4 months, females are able to live in adult state for more than a year. The dierent life spans result in a sex ratio skewed toward females throughout the whole year. Although the sex-ratio in Calanus glacialis CV is close to equilibrium within the same year class (CV sex-ratio in October is 0.7 male per female, Table 3), it shifts dramatically to 0.2 when both sexes achieve adulthood (Table 3). This decrease of the male proportion seems to be mostly related to the presence of a high proportion of old females in the population and much shorter life spans of the adult males. The life cycle of Calanus glacialis in the White Sea is well tuned to the strong seasonality of the environment, and its reproductive cycle is well scheduled to the annual periodicity of primary production. Similar to other large herbivorous copepods in polar waters, the reproductive
cycle of Calanus glacialis ensures that its ospring have reached active feeding stages by the time of maximum primary production in the water column. In this context, the long life spans of the females and their iteroparity represent an advantageous survival strategy for the species in a seasonally resource-restricted environment. Acknowledgements This research was supported by the Russian Foundation for Basic Research, RFBR grants 95-05-15424 and 9805-65426. I am especially indebted to Dr. N.M. Pertzova for providing the multiyear zooplankton collections for investigation of the Calanus gonads and fruitful discussions during preparation of the manuscript. The comments of Dr. H.-J. Hirche and two anonymous reviewers substantially improved the manuscript.
References Beklemishev KV, Valovaja NA, Ivanova VL, Mayer EM, Pantjulin AN, Semenova NL, Sergeeva OM (1975) New ideas on the oceanographic and biological structure of the White Sea (in Russian). Dokl Akad Nauk SSSR 224:209±211 Conover RJ (1988) Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiologia 167/168:127±142 Conover RJ, Sieferd TD (1993) Dark-season survival strategies of coastal zone zooplankton in the Canadian Arctic. Arctic 46:303±311 Drits AV, Pasternak AF, Kosobokova KN (1993) Feeding, metabolism and body composition of the Antarctic copepod Calanus propinquus Brady with special reference to its life cycle. Polar Biol 13:13±21 Fedorov VD, BobrovYuA (1977) Seasonal changes of some indices of productivity of the phytoplankton of the White Sea (in Russian). Izv Akad Nauk SSSR Ser Biol 1:104±112 Grainger EH (1963) Copepods of the genus Calanus as indicators of eastern Canadian waters. In: Dunbar MJ (ed) Marine distributions. R Soc Can Spec Publ 5:68±94 Grigg H, Bardwell SJ (1982) Seasonal observations on moulting and maturation in Stage V copepodites of Calanus ®nmarchicus from the Firth of Clyde. J Mar Biol Assoc UK 62:315±328 Grigg H, Bardwell SJ, Tyzack S (1981) Patterns of variation in the prosome length of overwintering stage V copepodites of Calanus ®nmarchicus in the Firth of Clyde. J Mar Biol Assoc UK 61:885±899 Grigg H, Holmes LJ, Bardwell SJ (1985) Seasonal observations on the biometry and development in copepodite stage V of Calanus ®nmarchicus from the Firth of Clyde. Mar Biol 88:73±83 Hagen W, Schnack-Schiel SB (1996) Seasonal lipid dynamics in dominant Antarctic copepods: energy for overwintering or reproduction? Deep Sea Res 43:139±158 Hirche H-J (1989) Egg production of the Arctic copepod Calanus glacialis ± laboratory experiments. Mar Biol 103:311±318 Hirche H-J, Bohrer RN (1987) Reproduction of the Arctic copepod Calanus glacialis in Fram Strait. Mar Biol 94:11±17 Hirche H-J, 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 117:615±622 Hirche H-J, Kwasniewski S (1997) Distribution, reproduction and development of Calanus species in the Northeast Water in relation to environmental conditions. J Mar Systems 10:299±317 Hirche H-J, Nieho B (1996) Reproduction of the Arctic copepod Calanus hyperboreus in the Greenland Sea ± ®eld and laboratory observations. Polar Biol 16:209±219 Hirche H-J, Hagen W, Mumm N, Richter C (1994) The Northeast Water Polynya, Greenland Sea. III. Meso- and macrozooplankton distribution and production of dominant herbivorous copepods during spring. Polar Biol 14:491±503
263 Huntley M, Strong KW, Dengler AT (1983) Dynamics and community structure of zooplankton in the Davis Strait and Northern Labrador Sea. Arctic 36:143±161 Jaschnov WA (1955) Morphology, distribution and systematics of Calanus ®nmarchicus s.l. (in Russian). Zool Zh 34:1210±1223 Jaschnov WA (1966) Water masses and plankton. 4. Calanus ®nmarchicus and Dimophyes arctica as indicators of the Atlantic waters in the Polar Basin (in Russian). Okeanologiya 6:493±503 Jaschnov WA (1970) Distribution of Calanus species in the Seas of the Northern Hemisphere. Int Rev Ges Hydrobiol 55:197±212 Kokin KA, Koltzova TI (1972) To the study of phytoplankton of the White Sea (in Russian). In: Complex investigation of the nature of the ocean, vol 3. Moscow University, Moscow, pp 153±162 Kosobokova KN (1981) Zooplankton of the Central Arctic Basin (in Russian). PhD Thesis, PP Shirshov Institute of Oceanology, Moscow Kosobokova (1986) Estimation of production of common herbivorous copepods of the Central Arctic Basin. Oceanology 26:749±752 Kosobokova KN (1990) Age-related and seasonal changes in the biochemical makeup of the copepod Calanus glacialis Jaschnov as related to the characteristics of its life cycle in the White Sea. Oceanology 30:103±109 Kosobokova KN (1993) Reproduction and egg production of the White Sea copepod Calanus glacialis under experimental conditions. Oceanology 33:337±340 Kosobokova KN (1994) Reproduction of the calanoid copepod Calanus propinquus in the Southern Weddell Sea, Antarctica: observations in the laboratory. Hydrobiologia 292/293:219±227 Kosobokova KN, Pertzova NM (1990) Biology of the Arctic copepod Calanus glacialis in the White Sea (in Russian). In: Vinogradov ME (ed) Biological monitoring in coastal waters of the White Sea. IOAN, Moscow, pp 57±71 Lehninger AL (1975) Biochemistry. North, New York Maclellan DC (1967) The annual cycle of certain calanoid species in West Greenland. Can J Zool 45:101±115 Marshall SM, Orr OP (1955) The biology of a marine copepod Calanus ®nmarchicus Gunnerus. Oliver & Boyd, Edinburgh Melle W, Skjoldal HR (1998) Reproduction and development of Calanus ®nmarchicus, C. glacialis and C. hyperboreus in the Barents Sea. Mar Ecol Prog Ser 169:211±228 Miller CB, Cowles TJ, Wiebe PH, Copley NJ, Grigg H (1991) Phenology in Calanus ®nmarchicus (Gunnerus): hypotheses about control mechanisms. Mar Ecol Prog Ser 72:79±91 Nieho B (1998) The gonad morphology and maturation in Arctic Calanus species. J Mar Systems 15:53±59 Nieho B, Hirche H-J (1996) Oogenesis and gonad maturation in the copepod Calanus ®nmarchicus and the prediction of egg production from preserved samples. Polar Biol 16:601±612 Norrbin MF (1991) Gonad maturation as an indication of seasonal cycles for several species of small copepods in the Barents Sea. Polar Res 10:421±432 Norrbin MF (1993) Skewed sex ratios in overwintering copepodites of Pseudocalanus in Norwegian fjords ± a result of sex-speci®c selection? Bull Mar Sci 53:204±215 Norrbin MF (1994) Seasonal patterns in gonad maturation, sex ratio and size in some small, high-latitude copepods: implications for overwintering tactics. J Plankton Res 16:115±131 Pavshtiks EA (1977) Seasonal variations in the age composition of copepod populations (Calanoida) in the Arctic Basin (in Russian). Exploration of the fauna of the seas 19:56±73
Pertzova NM (1971) On the quantitative vertical distribution of zooplankton in the Kandalaksha Bay of the White Sea (in Russian). In: Pertzov NA (ed) Complex investigation of the nature of the ocean. Moscow University, Moscow, pp 153±162 Prygunkova RV (1968) On the cycle of development of Calanus (Calanus glacialis Jaschnov) in the White Sea (in Russian). Doklady Akademii nauk USSR 182:1447±1450 Prygunkova RV (1974) Certain peculiarities in the seasonal development of zooplankton in the Chupa Inlet of the White Sea (in Russian). Exploration of the fauna of the seas 13:4±55 Runge JA (1987) Measurement of egg production rate of Calanus ®nmarchicus from preserved samples. Can J Fish Aquat Sci 44:2009±2012 Runge JA, McLaren IA, Corkett CJ, Bohrer RN, Koslow JA (1985) Molting rates and cohort development of Calanus ®nmarchicus and C. glacialis on the sea o southwest Nova Scotia. Mar Biol 86:241±246 Safronov SG (1984) Ecology of the copepod Calanus glacialis from the Sea of Okhotsk (in Russian). Sov J Mar Biol 10:200±203 Schnack-Schiel SB, Hagen W (1995) Life-cycle strategies of Calanoides acutus, Calanus propinquus and Metridia gerlachei (Copepoda, Calanoida) in the eastern Weddell Sea, Antarctica. ICES J Mar Sci 52:541±548 Smith SL (1990) Egg production and feeding by copepods prior to the spring bloom of phytoplankton in Fram Strait, Greenland Sea. Mar Biol 106:59±69 Smith SL, Lane PVZ (1991) The jet o Point Arena, California: its role in aspects of secondary production in the copepod Eucalanus californicus Johnson. J Geophys Res 96:14948±14958 Smith SL, Schnack-Schiel SB (1990) Polar zooplankton. In: Smith WO (ed) Polar oceanography. Part B: chemistry, biology, and geology. Academic Press, New York, pp 527±598 Spiridonov VA, Kosobokova KN (1997) Winter ontogenetic migrations and the onset of gonad development in large dominant calanoid copepods in the Weddell Gyre (Antarctica). Mar Ecol Prog Ser 157:233±246 Tande KS (1989) Calanus in North Norwegian fjords and in the Barents Sea. In: Sakshaug E, Hopkins CCE, éritsland NA (eds) Proceedings of the Pro Mare Symposium on Polar Marine Ecology. Polar Res 10:389±407 Tande KS, Gronvik S (1983) Ecological investigations on the zooplankton community of Balsfjorden, Northern Norway: sex ratio and gonad maturation cycle in the copepod Metridia longa (Lubbock). J Exp Mar Biol Ecol 71:43±54 Tande KS, Hopkins CCE (1981) Ecological investigations of the zooplankton community of Balsfjorden, northern Norway: genital system in Calanus ®nmarchicus and the role of gonad development in the overwintering strategy. Mar Biol 63:159±164 Tande KS, Hassel A, Slagstad D (1985) Gonad maturation and possible life cycle strategies in Calanus ®nmarchicus and Calanus glacialis in the northwestern part of the Barents Sea. In: Gray JS, Christiansen ME (eds) Marine biology of polar regions and eects of stress on marine organisms. Wiley, Chichester, pp 141±155 Timonov VV (1950) Major characters of the hydrological regime of the White Sea (in Russian). To the memory of Y.M. Shokal'ksy Moscow-Leningrad: Izd. AN SSSR, pp 206±236 Tourangeau S, Runge JA (1991) Reproduction of Calanus glacialis under ice in spring in southeastern Hudson Bay, Canada. Mar Biol 108:227±233 Vervoort W (1951) Plankton copepods from the Atlantic sector of the Antarctic. K Ned Akad Verh Afd Natuurkd Tweede Reeks 48:1±156
