Seasonal development of Calanus finmarchicus in relation to phytoplankton bloom dynamics in the Norwegian Sea

Transcription

1 Deep-Sea Research II 54 (2007) Seasonal development of Calanus finmarchicus in relation to phytoplankton bloom dynamics in the Norwegian Sea Cecilie Broms, Webjørn Melle Institute of Marine Research, P.O. Box 1870 Nordnes, N-5817 Bergen, Norway Received in revised form 29 July 2007; accepted 11 August 2007 Available online 22 October 2007 Abstract Seasonal development of Calanus finmarchicus was studied in relation to the physical environment and phytoplankton bloom dynamics in the Norwegian Sea during eight basin-scale surveys from March to August Our main objective was to gain new knowledge about the life cycle of C. finmarchicus and its adaptation to the physical and biological environment of the Norwegian Sea. Time of spawning, estimated by temperature-dependent back-calculations from the occurrences of copepodite stage 1 (CIs), varied by water mass and occurred mainly during the phytoplankton pre-bloom and bloom periods. Recruitment to CI of the year s first generation (G1) generally occurred during the bloom and late bloom. The seasonal development of C. finmarchicus was progressively delayed from Coastal to Atlantic and to Arctic water, and from south to north within Atlantic and Arctic waters. This delay was partly linked to the phytoplankton bloom development that followed the same pattern, but development of C. finmarchicus also showed an increasing tendency to lag behind the phytoplankton development in colder waters. This may explain why C. finmarchicus are less successful in colder water. The consumption of nitrate was used as proxy for the seasonal history of phytoplankton development to aid interpretation of the lifecycle of C. finmarchicus. This approach allows us to align phytoplankton bloom and copepod development sequences despite temporal and geographical variation in bloom development, which otherwise tend to cause variability in quasi-synoptic and large-scale data. Two generations of C. finmarchicus were found in southern and northern regions of Coastal Water, and in southern Atlantic Water. In northern Atlantic Water and in Arctic Water, one generation was observed. r 2007 Elsevier Ltd. All rights reserved. Keywords: Calanus finmarchicus; Life cycle; Phytoplankton development; Nitrate; Chlorophyll; Norwegian Sea 1. Introduction The upper layers of the Norwegian Sea contain three water masses: Coastal Water over the Norwegian Shelf, Atlantic Water and Arctic Water. Each Corresponding author. Tel.: ; fax: address: cecilie.broms.aarnes@imr.no (C. Broms). has characteristic physical, chemical and biological features (Skjoldal, 2004). The Atlantic Water enters the Norwegian Sea mainly through the Faroe Island Shetland channel and is relatively warm and saline (Blindheim, 2004). The colder and less saline Arctic Water dominates the western Norwegian Sea, separated from Atlantic Water by the Arctic Front. The Front is situated above the Mohn Ridge north of Jan Mayen. South of Jan Mayen, /$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi: /j.dsr

2 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Arctic Water enters the southwestern Norwegian Sea as the East Icelandic current. The strength and eastward extension of the current varies with the hydrographic and atmospheric conditions, as does the position of the Arctic Front (Blindheim, 2004). Over the Norwegian Shelf east of the Atlantic Water, Coastal Water flows northwards. Coastal Water is less saline than Atlantic Water, and its temperature is warmer during summer and colder during winter. The front between Atlantic and Coastal Water is usually situated above the shelf break but moves westward during periods of northerly winds. The initiation of the phytoplankton spring bloom varies between oceanographic regions of the northeastern Atlantic (Paasche, 1960; Dale et al., 1999; Rey, 2004; Gaard et al., 2006). In the Norwegian Sea, the spring bloom starts in Coastal Water and occurs later in Atlantic and Arctic waters (Rey, 2004). In Atlantic Water, the pre-bloom period starts in early March and develops through April, and the spring bloom phase starts in early May with a post-bloom period following immediately (Rey, 2004). The bloom in Coastal waters starts in April, but a high-resolution time series of a complete bloom cycle is lacking for this water mass (Gaard et al., 2006). Variation in the timing of the bloom within water masses is less pronounced, based on satellite data (Rey, 2004) and in situ chlorophyll data from within water masses (e.g. Gaard et al., 2006). The Norwegian Sea has been described as a predictable environment (Ferno et al., 1998) with strong seasonality in phytoplankton production, which is mainly related to variation among water masses. The seasonal cycle of zooplankton production is closely related to the phytoplankton spring bloom (Diel and Tande, 1992; Melle and Skjoldal, 1998; Niehoff et al., 1999; Niehoff and Hirche, 2000; Melle et al., 2004) and will therefore differ among the water masses. This relationship to the phytoplankton bloom also is reflected in an early start of zooplankton production in the south-eastern Norwegian Sea and a delay towards the northwest (Pavshtiks, 1956; Melle et al., 2004). Calanus finmarchicus is the dominant zooplankton in the Norwegian Sea (Wiborg, 1955; Timokhina, 1964; Melle et al., 2004) and an important prey of several planktivorous fish stocks, including Norwegian spring spawning herring (Jespersen, 1932; Dalpadado et al., 2000; Gislason and Astthorsson, 2002; Dommasnes et al., 2004). They overwinter in deep water, and ascend to surface waters to spawn in early spring (Østvedt, 1955; Niehoff et al., 1999; Melle et al., 2004; Stenevik et al., 2007). When the new generation reaches the overwintering stages (mainly the fifth copepodite stage) in mid to late summer, they either descend to overwintering depths, or mature to produce a second generation (Conover, 1988; Melle et al., 2004). A 1-year life cycle is predominant in most of the Norwegian Sea, while two or more generations per year may be found in the southern and eastern parts (Wiborg, 1954; Østvedt, 1955; Matthews et al., 1978; Melle et al., 2004). Most of the information about the timing of the phytoplankton bloom and production of C. finmarchicus in relation to water masses is obtained from time series sampling at single stations or single cruises covering more than one water mass. Detailed studies on a basin-scale with sufficient temporal sampling resolution within water masses are still needed to confirm and expand our present understanding of the seasonal development of the plankton. The present investigation is unique with respect to the basin-scale nature of our data, which also span the major part of the productive season of the Norwegian Sea. Large areas of the Norwegian Sea, including Coastal, Atlantic and Arctic waters, were covered from March to August. Data on physics, nutrients, chlorophyll-a and demography of C. finmarchicus were included in the study. During the same cruises, information concerning distribution, biology and diet of the Norwegian spring spawning herring were gathered. A subsequent paper will deal with the feeding migration and diet of Norwegian spring spawning herring in relation to the seasonal cycle of C. finmarchicus in the Norwegian Sea. The aims of this investigation were (1) to describe the seasonal dynamics of the phytoplankton in relation to the physical characteristics of water masses and (2) to relate the timing of the ascent, spawning, ontogenetic development and generational cycles of C. finmarchicus to the phytoplankton development. Our main objective was to gain new knowledge about the life cycle of C. finmarchicus, and its adaptation to the physical and biological environment of the Norwegian Sea. 2. Material and methods Eight cruises were carried out in the Norwegian Sea from March to August 1995 with the RVs

3 2762 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) G.O. Sars, Johan Hjort and Michael Sars (Fig. 1). Hydrographic data and water samples for determination of nutrients and chlorophyll-a concentrations were collected at a total of 408 stations by vertical casts using a CTD with water bottles mounted. Laboratory analyses of nutrients and chlorophyll-a were performed according to Melle and Skjoldal (1998). The sampling stations were classified into three water masses based on salinity at 20 m and geographical position in relation to the central water mass, i.e. Atlantic Water: Coastal Water (salinity o35, sample position east of the Atlantic water mass), Atlantic Water (salinity 4 ¼ 35), and Arctic Water (salinityo35, sample position west of the Atlantic water mass). The stage of the phytoplankton bloom in individual samples and regions, relative to the overall seasonal bloom sequence, was assessed using values of nitrate and chlorophyll-a at 20 m, calculations of consumed nitrate (integrated assumed winter values of nitrate in the upper 100 m minus the integrated nitrate in the upper 100 m), and integrated chlorophyll-a in the upper 100 m of the water column. At several stations the observed maximum nitrate values were above the usual assumed winter values of 12 mmol l 1 in Atlantic Water and 10 mmol l 1 in Coastal Water (Rey, 2004). The highest nitrate value observed for each water mass was therefore taken to be the winter level when estimating the nitrate consumption. Chlorophyll-a values from 0.25 to 0.50 mg m 3 were taken to represent a pre-bloom situation and values above 0.50 mg m 3 a bloom situation. The late bloom was assumed to occur immediately after the bloom (Rey, 2004). Fig. 1. Map of study area. Six cruises were conducted on the following dates: 1 21 March (RV G.O. Sars), April (RV G.O. Sars), 27 April 24 May (RV Johan Hjort), 26 May 22 June (RV G.O. Sars), 7 July 2 August (RV Johan Hjort), and 29 July 15 August (RV G.O. Sars). Circles represent hydrography, nitrate, chlorophyll-a and zooplankton stations. In addition hydrography, nitrate and chlorophyll-a data were collected at a number of stations during the cruises (not shown in figure, see Table 1). Additionally, two standard sections through Coastal and Atlantic waters were sampled 9 May (RV G.O. Sars), heading NW, starting at 68.51N, 13.81E, and June (RV Michael Sars), heading NW, starting at 62.41N, 5.21E. Solid black lines indicate the location of the 35 isohaline at 20 m depth based on combined salinity values from June and July, using kriging as the interpolation method. The isohalines do not represent the exact position of the Atlantic and Arctic fronts for the whole sampling period, and were not used for classification of stations according to water mass (see Section 2).

4 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) A total of 96 zooplankton stations was sampled during the surveys. The zooplankton samples were collected by oblique hauls, from the bottom or 700 m to the surface, with a 1-m 2 MOCNESS (Wiebe et al., 1985). The MOCNESS was equipped with eight 180-mm mesh nets and, in the present study, samples from the four shallowest nets, , , and 25 0 m, were analysed. During the surveys, the zooplankton samples were divided in two. One half was preserved in formaldehyde and later analysed to lowest taxonomic level possible at the Institute of Marine Research, Bergen, Norway. For Calanus spp., individuals also were identified and counted to copepodite stage and adult sex. All MOCNESS samples were integrated over depth and all Calanus data are presented as #m 2. The other half of each sample was used for biomass estimation (not presented here). The date-in-year of spawning (D s )byc. finmarchicus was back-calculated from observed abundances of copepodite stage 1 (CI). The following temperature-dependent relationship (Corkett et al., 1986) was used for back-calculation: D s ¼ D CI ð1408 n ðt average þ 7:36Þ ð 1:64Þ Þ, (1) where D CI ¼ day of the year for observation of CI, and T average ¼ average temperature that influenced the CIs from when they were spawned to their development into CI. For estimation of T average the Norwegian Sea was divided into five regions; southern (south of 691N) and northern (north of 691N) Coastal- and Atlantic waters, and Arctic Water. T average was calculated as follows: T average ¼ ðd 1T 1 þ d 2 T 2 þ...þ d n T n Þ, (2) ðd 1 þ d 2 þ...þ d n Þ where T 1,y,T n ¼ the average temperature for each region in the Norwegian Sea calculated for all eight cruises, and d 1, y,d n ¼ the number of days each specimen was exposed to the different region and cruise specific temperatures. A standardized index of the ratio between abundance of CVI females and CV [(CVI females CV)/(CVI females+cv); Diel and Tande, 1992] was calculated for the population analyses. An index of +1 indicates that all specimens are adult females and 1 that all specimens are CV. The mean copepodite stage index of C. finmarchicus was used in regression analyses to reveal differences in the seasonal development within water masses. The mean stage index does not represent the mean stage of C. finmarchicus in a given area, since duration of each copepodite stage differs (Aksnes and Blindheim, 1996 and references therein), but is an indicator for the seasonal development of C. finmarchicus. The index is dependent on temperature and food availability, due to the temperature- and food-dependent growth and copepodite stage duration showed by C. finmarchicus (Corkett et al., 1986; Harris et al., 2000). 3. Results 3.1. Physical environment and phytoplankton development Mean temperature within water masses increased through the season. Seasonal changes in temperatures were similar in southern Coastal and Atlantic water masses. For both water masses, temperature was higher in southern compared with northern regions. Lowest temperatures were found in Arctic Water (Table 1). In March, nitrate concentrations were close to winter values both in Coastal and Atlantic waters (Table 2). Average chlorophyll-a concentrations were above winter levels in both water masses, and in Coastal Water phytoplankton development was characterised as pre-bloom (Table 2). In April, increases in chlorophyll-a concentrations were found with values indicating a pre-bloom situation in Coastal, Atlantic and Arctic waters. In May significant increases in chlorophyll-a concentrations were found in all water masses, and especially in Coastal Water. A decrease in nitrate concentrations also had taken place; these results together indicated a phytoplankton spring bloom situation. At the end of May and in June the bloom had ended in Coastal Water. In Arctic Water, however, chlorophyll-a values were high, indicating a phytoplankton bloom. In June at the westernmost stations in Arctic Water near Jan Mayen, chlorophyll-a concentrations varied from 2.47 to 7.78 mg m 3 and nitrate concentrations from 1.17 to 8.53 mmol l 1. The phytoplankton bloom development thus seemed more advanced compared with the remaining Arctic area (Table 2). Throughout July and August, nitrate concentrations were low in all water masses. Integrated chlorophyll-a and the consumption of nitrate in the upper 100 m of the water column were studied in north south and east west directions within the water masses to reveal potential gradients

5 2764 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Table 1 Average temperatures (1C) and salinity for cruise-specific water masses and regions in the Norwegian Sea from March to August 1995 Cruise period Water mass Region Temperature Salinity n Mean SD n Mean SD 1 21 March Coastal South Coastal North Atlantic South Atlantic North April Coastal South Atlantic South Arctic April 24 May Coastal South Coastal North Atlantic South Atlantic North Arctic May 27 June Coastal South Coastal North Atlantic South Atlantic North Arctic July 2 August Coastal South Coastal North Atlantic South Atlantic North Arctic July 15 August Coastal South Coastal North Atlantic South Atlantic North Arctic in the phytoplankton bloom development within each water mass. In Coastal Water, there was a negative correlation between integrated chlorophylla and latitude in March, and a positive correlation in July and August (linear regressions of integrated chlorophyll-a on latitude, Po0.05, n ¼ 22, 34, 27). A positive correlation with latitude also was found for consumed nitrate in July (linear regression, Po0.05, n ¼ 34). In Atlantic Water, integrated chlorophyll-a was negatively correlated with latitude in March, and consumed nitrate was negatively correlated with latitude in March and May (linear regressions, Po0.05, n ¼ 24, 71). In Arctic water masses, integrated chlorophyll-a was negatively correlated with latitude in May (linear regression, Po0.05, n ¼ 48). No north south gradients in nitrate consumption were found in Arctic Water (linear regressions, P40.05). In several periods and in all water masses there was a significant relationship between chlorophyll-a and nitrate consumption vs. longitude (linear regressions, Po0.05). This is probably related to the north south direction of fronts in the Norwegian Sea (Fig. 1) and our choice of a fixed and abrupt classification boundary (salinity 35) between water masses, while changes in environmental conditions towards the fronts are gradual. Due to the north south gradients in the progress of the phytoplankton spring bloom during some periods, Coastal and Atlantic water masses were further subdivided into southern (south of 691N) and northern (north of 691N) subregions to gain unambiguous and region-specific results. Samples from the Arctic water mass were not divided into subregions, owing to too few sampling stations. Time series were used to examine the sequential changes of integrated chlorophyll-a and consumed nitrate in the different regions during the season. In both southern and northern regions in Coastal and

6 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Table 2 Average concentrations of chlorophyll-a (mg m 3 ) and nitrate (mm) in different water masses in the Norwegian Sea from March to August 1995 Cruise period Water mass Chlorophyll a 20 m Atlantic Water, a peak in integrated chlorophyll-a was observed in early May (Fig. 2A, C, E, G). In Arctic Water, however, maximum integrated chlorophyll-a values were found in the second half of May and early June (Fig. 2I). All regions showed an increase in consumed nitrate during the season. In Coastal Water (Fig. 2A, C) and in the southern region of Atlantic Water (Fig. 2E), there had been a noticeable consumption of nitrate in March, with maximum consumptions of mmol m 2. In the northern region of Atlantic Water (Fig. 2E, G) and in Arctic Water (Fig. 2I), these amounts of consumed nitrate were not found until the first and second half of May, respectively. Note that the northern Atlantic Water was not sampled in April. The large variability of the timespecific amount of consumed nitrate found in all regions may be due to sampling stations near the Atlantic and Arctic fronts, consisting of mixed water masses C. finmarchicus seasonal development Nitrate 20 m n Mean SD Mean SD 1 21 March Coastal Atlantic April Coastal Atlantic Arctic April 24 May 26 May 27 June 7 July 2 August 29 July 15 August Coastal Atlantic Arctic Coastal Atlantic Arctic Coastal Atlantic Arctic Coastal Atlantic Arctic In Coastal Water, the overwintering generation of C. finmarchicus (G0) started to enter the upper 200 m of the water column in March, although the concentrations (individuals m 2 ) were low (Table 3). The production of copepodite stage 1 (CI) of the first generation (G1) started in March, but remained low until May when large increases in the numbers of the young copepodite stages (CI CIII) occurred. The individuals of G0 that produced G1 in May did not show up in our samples from Coastal Water, except in very small numbers during March and April. In Coastal Water in June high numbers of both young and old (CIV CVI) copepodite stages were observed. The older stages probably belonged to G1 at this time. The concentration of all stages decreased through July and August, except in August when secondary peaks of stages CIII and CIV were found. In Atlantic Water, the overwintering generation was found in March, but in low numbers (Table 3). The concentration of all stages belonging to G0 increased considerably in April and May. In May, the mean number of individuals in G0, stages CIV to CVI, was estimated at about m 2. The production of CI of G1 had barely started in April, and the presence of relatively large numbers of adult males in April and May indicated that reproduction was not finished. The small proportion of CIIIs found in Atlantic Water in April probably had remained in the surface water near the Arctic Front during winter. The main increase in the numbers of the young copepodite stages in Atlantic Water took place in June, and was delayed compared with Coastal Water. High numbers of old stages in June, July and August probably belonged to G0 and G1, but separation of generations based on the data in Table 3 is difficult. The concentration of CVs was reduced in August, and the concentration of CVIs was reduced in July and August, representing development into older stages and descent of the overwintering stages. The large number of younger copepodite stages in Atlantic Water in August was due to high concentrations at the northernmost stations (not shown). In Arctic Water, high numbers of G0 were found in April (Table 3). A small proportion of younger stages also were found, probably belonging to G0. The relative stage composition was similar in Atlantic and Arctic water masses in April, but copepodites in Arctic Water outnumbered those in Atlantic Water for all stages. A small increase in the number of CIs of G1 was found in June, but CVs dominated Arctic Water in June and July. The numbers of young stages observed throughout the

7 2766 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Fig. 2. Depth-integrated chlorophyll-a and consumption of nitrate (0 100 m) (A, C, E, G, I), and C. finmarchicus population characteristics: abundance of CI, back-calculated time of spawning and copepodite stage ratio index (B, D, F, H, J) in Coastal, Atlantic and Arctic waters. Southern regions are defined as south of 691N and northern regions as north of 691N.

8 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Table 3 Average abundance (individuals m 2 )ofcalanus finmarchicus copepodite stages in different water masses from March to August 1995 in the Norwegian Sea Water mass Cruise periods n CI CII CIII CIV CV CVIf CVIm Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD Coastal 1 21 March April April 24 May 2 36,960 51,396 22,953 31,529 19,149 26, May 27 June 3 35,906 54,871 53,099 75,910 84,105 95, ,961 53,176 16, July 2 August 7 10,703 14,607 11,571 15, ,236 13, July 15 August ,619 16,873 29,893 25,276 41, Atlantic 1 21 March April ,230 10, ,863 13, April 24 May ,368 28,121 24, ,746 17, May 27 June 12 18,961 48,161 18,693 42,099 15,089 30,880 22,991 41,384 24,365 21,193 20,078 15, July 2 August , ,521 16,308 15,814 41,709 42, July 15 August 9 628,051 14,958 58,875 91, ,661 45,470 20,475 30, Arctic April ,966 48,911 26,788 13,822 25,198 12, April 24 May , May 27 June ,426 10,881 17,388 13, July 2 August ,631 22, July 15 August , CVIf ¼ copepodite stage VI female, CVIm ¼ copepodite stage VI male. season in Arctic Water were low in comparison to the high abundance of G0 found in April. The copepodite mean stage index of C. finmarchicus was studied in north south and east west directions within each water mass to reveal potential gradients in the seasonal development. No significant north south or east west differences of the stage composition of C. finmarchicus were found within Coastal Water (linear regression of mean stage index of C. finmarchicus on latitude, P40.05). In Atlantic Water, however, an increase in the mean stage index with latitude in June and a decrease in the index in July and August (Po0.05, n ¼ 12, 14, and 9, respectively) were found. During April in Atlantic Water, the mean stage index of C. finmarchicus was positively related to longitude (Po0.05, n ¼ 6). In Arctic Water, the mean stage index was positively related to latitude in June, and negatively related to longitude in April (Po0.05, n ¼ 5, 4). Due to these gradients in the seasonal development of C. finmarchicus found within water masses, further division of Coastal and Atlantic water masses into northern and southern subregions was adopted for additional analyses of spawning and development of C. finmarchicus. Time series of the abundance of C. finmarchicus CIs, back-calculated spawning time and stage ratio index between the numbers of CVI female and CVs were examined and compared to the seasonal phytoplankton development (Fig. 2). In the southern subregion of Coastal Water, the stage ratio index reached highest values in the middle of March, with a following spawning peak in the middle of April and recruitment to CI of G1 in the beginning of May (Fig. 2B). The peak in CI abundance co-occurred with the peak in chlorophyll-a. A secondary peak in spawning and recruitment to CI was found in July. The stage ratio index, however, decreased steadily throughout the season. In the northern region of Coastal Water, peaks in spawning and recruitment to CI of G1 were found in May and June, respectively. The spawning occurred immediately after the maximum of integrated chlorophyll-a (Fig. 2C, D). However, due to lack of Calanus data prior to early June, information is lacking on the initiation of the production of G1 in this region. In the southern region of Atlantic Water, the stage ratio index peaked in the second half of April, and then decreased throughout the season (Fig. 2F). The spawning and recruitment to CI occurred in the first half of June, after the peak in the phytoplankton bloom. Earlier recruitment to CI from mid-may to mid-june cannot be excluded because of uncertainty due to a gap in our time series. In the northern region of Atlantic Water, the stage ratio index indicated an even mixture of CVI females and CVs in May and June and still many CVs in August.

9 2768 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Together with the occurrence of CIs, this suggests a first recruitment to G1 after mid-june and continuing production of G1 in August. Based upon the progress of the stage ratio index, spawning was not synchronised within the population and occurred after the phytoplankton bloom (Fig. 2G, H). In Arctic Water, the highest observed stage ratio index was at the end of April (Fig. 2I). Spawning was estimated to occur at the end of May and co-occurred with the bloom. Recruitment to CI was found in late June, just after the peak in chlorophyll-a. Time series of C. finmarchicus, chlorophyll-a and nitrate consumption revealed differences in the timing of events between water masses and regions. This implies differences in how reproduction and recruitment of C. finmarchicus are linked to phytoplankton development. However, there are gaps in the time series, and regions are heterogeneous with respect to timing of events, although division into water masses and subdivision by latitude were used to reduce heterogeneity. Therefore, data were further explored to describe better the link between seasonal phytoplankton development and C. finmarchicus reproduction and generational cycle. For this, nitrate consumption was introduced as another proxy for the stage of development of the phytoplankton bloom. Nitrate consumption is linked to the seasonal history of cumulative production by phytoplankton. Its use may reduce the problem of heterogeneity within the regions where different stages of the bloom were encountered at approximately the same time Relationships between consumed nitrate, phytoplankton development and the seasonal cycle of C. finmarchicus The relation between integrated chlorophyll-a and consumption of nitrate was explored to evaluate the suitability of nitrate consumption as proxy for cumulative phytoplankton bloom development. Although, significant positive linear relationships were found between the consumption of nitrate and integrated chlorophyll-a concentrations, except for northern region of Coastal Water (Fig. 3), nitrate consumption explained only 4 17% of the variations in integrated chlorophyll-a. This is probably because the expected relationship between chlorophyll-a and nitrate consumption is domeshaped, when pre-, bloom and post-bloom situations are all included. Fig. 3 indicates a peak in integrated chlorophyll-a at intermediate concentrations of consumed nitrate. The short duration of the bloom (Fig. 2) may cause difficulties in relating the life cycle of C. finmarchicus to high concentrations of chlorophyll-a. Consumption of nitrate, which increases steadily throughout the season within regions (Fig. 2), was thus adopted as proxy for phytoplankton seasonality in the Norwegian Sea. Fig. 4 summarises the seasonal development of C. finmarchicus in Coastal, Atlantic and Arctic waters. In the southern subregion of the Coastal Water, two peaks in the abundance of CI CIII were found. These peaks probably belonged to G1 and G2, indicating two generations per year. In the northern subregion of Coastal Water, the first peak in CI CIII was probably not sampled by our surveys. The increase in young stages therefore most likely belonged to G2, again suggesting two generations per year. South in Atlantic Water, also two generations were found, although the peaks in abundance of CI CIII were less pronounced than in southern Coastal Water. In northern Atlantic Water and in Arctic Water, one peak in the concentration of CI CIII was found, indicating a single generation per year in these regions. Despite the differences in timing and number of generations per year, when copepod development was related to the consumption of nitrate, several similarities in the life cycle of C. finmarchicus were found between the different regions in the Norwegian Sea (Fig. 4). The ascent of G0 was found at a consumption of mmol nitrate m 2, represented by large peaks in the concentration of CIV in southern Coastal Water and Arctic Water, and less pronounced peaks of older stages in Atlantic Water. North in Coastal Water G0 was probably not sampled. The subsequent peak concentration of CI CIIIs belonging to G1 were found at mmol consumed nitrate m 2 in all regions, except in the northern subregion of Coastal Water, where CI CIII of G1 were again probably missed by our sampling programme. The second peak of older stages, representing G1, was found at about 450 mmol consumed nitrate m 2 in most regions. An example of this is the peak in CVs at 450 mmol consumed nitrate m 2 in southern Coastal Water. A second peak in CI CIIIs, belonging to G2, was found in southern and northern Coastal Water and in southern Atlantic Water, all at a consumption of mmol nitrate m 2. Older and young copepodite stages within G2 had considerable time overlap.

10 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Fig. 3. Integrated chlorophyll-a vs. consumption of nitrate (0 100 m). Linear regression: Coastal Water south, R 2 ¼ 0.042, Po0.05, N ¼ 96, Coastal Water north, R 2 ¼ 0.14, P40.05, N ¼ 25, Atlantic Water south, R 2 ¼ 0.12, Po0.05, N ¼ 120. Atlantic Water north, R 2 ¼ 0.16, Po0.05, N ¼ 93, Arctic Water, R 2 ¼ 0.17, Po0.05, N ¼ Discussion The seasonal phytoplankton development occurred first in Coastal Water, then in Atlantic, and finally in Arctic Water (Table 2, Fig. 2). Chlorophyll-a values above winter levels were found in March in Coastal and Atlantic water masses, as observed by Dale et al. (1999) in Atlantic Water, indicating that the phytoplankton was no longer light limited. The prebloom was first initiated in Coastal Water in March, and in April in Atlantic and Arctic Water. The phytoplankton spring bloom was observed in May

11 2770 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Fig. 4. Mean abundance, by intervals of nitrate consumption, of C. finmarchicus copepodite stages I III (sum of stages I, II and III), IV, V and adult females vs. consumption of nitrate. Nitrate consumption is categorized with intervals of 100 mmol m 2. Standard deviations (SD) are not shown due to their large values. SD for the abundance of copepodite stages varied as follows. CI CIII: ,084 (9 242% of mean), CIV: ,819 (17 194% of mean), CV: ,892 (13 140% of mean), CVI females: ,196 (4 171% of mean). N ¼ 2 7. A total of 12 nitrate consumption intervals contained only one observation. Generalized additive models (Hastie and Tibshirani, 1990) (family ¼ poisson, link ¼ logit, df ¼ 4), fitted to the numbers of copepodites vs. consumed nitrate (observed values) revealed a similar course of events in the development of C. finmarchicus population, but the models showed no significant relationships between variations in the numbers of copepodites and consumed nitrate. The population development shown in the present figure must therefore not be seen as statistically significant. in all water masses; however, the main bloom persisted into June in Arctic Water, co-occurring with the culmination of the bloom in Coastal Water. Near Jan Mayen, the bloom occurred earlier than in the remaining areas of Arctic Water. This was caused by an earlier stratification of the water

12 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) column near Jan Mayen as indicated by lower salinity in the surface layers (data not shown). The differences in the timing of the phytoplankton spring bloom between Coastal, Atlantic and Arctic waters are due to differences in the mechanisms involved in water column stratification (Halldal, 1953; Paasche, 1960; Rey, 2004), a prerequisite for the phytoplankton bloom (Sverdrup, 1953). In Norwegian Coastal Water, a shallow mixed layer is maintained throughout the year over the shallow banks and at the front with the Atlantic Water, and the spring bloom starts as soon as surface irradiance increases sufficiently. In Atlantic and Arctic water masses, stratification is delayed until the spring increase in the daily solar radiation warms the upper water layer and causes development of a seasonal thermocline (Rey, 2004). This is a slower process and the bloom therefore occurs later than in Coastal Water (Paasche, 1960). The earlier bloom near Jan Mayen is a typical shelf bloom partly caused by similar mechanisms as described for Norwegian Coastal Water. Latitudinal differences in the timing of the seasonal phytoplankton development within water masses (linear regressions, Po0.05, see Section 3.1) were minor compared to the differences in timing between the water masses. When significant latitudinal differences within water masses were found, the chlorophyll concentration was negatively correlated with latitude at the beginning of the season (March May) and positively correlated at the end of the season (July August). This indicates that the phytoplankton spring bloom both started and ended earlier within the southern portion of the water masses, and then gradually extended northwards. However, differences within the water masses were small, as indicated by lack of north south differences in the phytoplankton development in most of the cruise periods. Previous investigations are ambiguous regarding north south differences in the bloom development in the Norwegian Sea. Latitudinal differences in the timing of the bloom have been found in Coastal Water (Braarud et al., 1958; Dale et al., 2001 and references therein). Rey (2004), on the other hand, reported no clear north south trend in the development of the bloom in the Norwegian Sea, and Gaard et al. (2006) concluded that there are only small differences in bloom timing within Norwegian Coastal Water. In the present investigation, the ascent of the overwintering generation of C. finmarchicus to the upper 200 m of the water column probably occurred during April in Atlantic and Arctic waters (Table 3). This conclusion is based on the large increase in the number of overwintering stages from March to April in Atlantic Water and high concentrations in April in Arctic Water. Only a small number of individuals belonging to the overwintering stages were found in Coastal Water in March and April. The shallow shelf is probably not an overwintering area for C. finmarchicus (Melle et al., 2004; Gaard et al., 2006), and the overwintering generation must therefore be advected on to the shelf from the deep Norwegian Sea or from the fjords (Slagstad and Tande, 1996; Melle et al., 2004). It is not yet clear whether advective recruitment to the shelf occurs mostly as G0 or as naupliar and copepodite stages of G1. Because of insufficient coverage in April, an advection to the shelf as G0 cannot be precluded. However, our data indicate that the advection of young copepodites may be significant. The present investigation and previous studies show minor differences in the timing of the termination of diapause and ascent to surface water between geographical areas and water masses in the Norwegian Sea. In the deep fjords in northern Norway the ascent starts in February and is completed in March and April (Sømme, 1934). Recruitment to Coastal Water is initiated in January and February, and the overwintering generation reaches peak surface-layer abundance in mid-april (Wiborg, 1954; Gaard et al., 2006). At weather station M (661N, 21E) in the Norwegian Sea, the upward migration starts in January, with highest abundance of the overwintering generation in surface water in the beginning of April (Østvedt, 1955; Hirche, 2001; Melle et al., 2004). Ascent that is simultaneous over as large an area as the Norwegian Sea suggests an endogenous long-range timer (Miller et al., 1991) as the mechanism controlling the arousal from diapause and ascent to surface water. In Atlantic Water, overwintering C. finmarchicus are found from 500 m to below 1000 m depth (Østvedt, 1955; Dale et al., 1999; Halvorsen et al., 2003; Melle et al., 2004). Very little light reaches these depths, so light intensity is not a plausible proximate cue initiating the ascent (Hind et al., 2000). The spawning dates of C. finmarchicus were backcalculated from time series observations of CI abundance. In Coastal Water, the back-calculations indicated that in southern parts, the main spawning by G0 took place in late April, immediately before the phytoplankton bloom (Fig. 2A, B). In northern

13 2772 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Coastal Water, the spawning by G0 was estimated to peak in mid-may, directly after the bloom peak (Fig. 2C, D). However, there is a lack of data before June. The high concentration of CI in the first half of June co-occurred with a low CVI female/cv ratio [the ratio starts decreasing when the spawning is initiated (Diel and Tande, 1992; Melle and Skjoldal, 1998)], suggesting that this was a late phase in the recruitment to CI of G1. We may therefore not have observed the peak spawning, and C. finmarchicus likely spawned during the bloom in mid-may (prior to the estimated peak spawning date). These interpretations are consistent with Stenevik et al. (2007) who have stated that phytoplankton development was in a late bloom situation in Coastal Water in May and females were still spawning at a considerable rate, but that the number of females was low. Our findings support the results of Diel and Tande (1992) who observed the main spawning during the April bloom in Coastal Water. In the southern portion of the Atlantic water mass, the highest spawning was estimated to be between late May and early June, after the bloom peak (Fig. 2E, F). Recruitment to CI of G1 in the pre-bloom was not observed and spawning during the pre-bloom and subsequent recruitment to CI in the bloom in May (Hirche et al., 2001; Melle et al., 2004) is thus likely. Niehoff et al. (1999) found that population spawning rates were equally high during the prebloom in April and the bloom period in May, while individual spawning rates where highest during the bloom in May. In northern Atlantic Water, spawning was estimated to occur in late July and CIs of G1 was observed in the first half of August, in a late bloom. However, a first recruitment to G1 after mid-june is possible based on observations of the occurrence of CIs and CVI females to CVs ratio. The bloom occurred simultaneously with the southern region (Fig. 2G, H. In Arctic Water the main spawning of G1 co-occurred with the bloom in late May (Fig. 2I, J). In the Norwegian Sea as a whole, spawning took place during the phytoplankton pre-bloom and bloom periods. Early spawning, in either the prebloom and bloom, may have several advantages. First, the spawning may be tuned to increase the chances of a match between the bloom and the early copepodite stages of the offspring generation. Second, the probability of the G1 offspring reaching an overwintering stage or producing a second generation also might increase through early spawning (Fiksen and Charlotti, 1998). Third, early spawning might reduce the risk for the parent generation of mortality due to predation of migrating fish, e.g. Norwegian spring spawning herring, which start to feed in the Atlantic water masses in April (Kaartvedt, 2000). On the other hand, the highest rate of egg mortality has been observed to be during the pre-bloom period (Ohman and Hirche, 2001). The seasonal development of C. finmarchicus was delayed from Coastal Water to Atlantic Water, and was further delayed in Arctic Water. In addition, a within water mass time lag in development was found from south to north within Atlantic and Arctic waters (linear regressions, Po0.05, Fig. 2). This delay was partly linked to the bloom development following the same pattern, but there was also a further delay of C. finmarchicus between the water masses and towards the north that exceeded variations in the bloom. A 1-month delay in the phytoplankton bloom was found between Coastal and Arctic waters (Fig. 2). The recruitment to CI of G1 was delayed by 1 2 months from Coastal to Arctic water, while a 2-month delay for recruitment to CIII was observed between the same water masses (Table 3, Fig. 2). This may be related to longer stage duration of C. finmarchicus in colder water (Table 1). Melle and Skjoldal (1998) observed that females in the Barents Sea matured and spawned after the bloom in the polar front region because of slower development in cold water, and suggested that this might be the reason why C. finmarchicus does not persist in colder water. Differences in the date of sampling must be taken into consideration in the interpretation of the stage composition between different parts of the Norwegian Sea. In May and June the survey direction was from north to south, and consequently, the northern part of the populations of C. finmarchicus were encountered earlier in the season. This may explain some of the developmental differences within Atlantic Water found at that time. However, in July and August, the survey direction was from south to north, but more advanced development was again found in the south. In Atlantic and Arctic water masses, at sampling stations near the Arctic Front (Fig. 1), low concentrations of CIII, probably belonging to G0, were observed at the beginning of the season. These individuals may have originated from a late spawning during the previous year and been able to survive the winter close to the surface. CIII has also been observed to be an overwintering stage in

14 C. Broms, W. Melle / Deep-Sea Research II 54 (2007) Atlantic Water in the Barents Sea (Melle and Skjoldal, 1998). The young individuals of G0 also could have been confused with C. glacialis, which may spawn earlier than C. finmarchicus in cold water (Melle and Skjoldal, 1998). However, C. glacialis is found only in very low numbers in the Norwegian Sea (Melle et al., 2004). A shallow overwintering depth of C. finmarchicus in the western Norwegian Sea is common for older stages, as well. This is probably associated with their tendency to overwinter in Arctic Intermediate water (Melle et al., 2004), which is denser than, and lies below, the Atlantic Water in the eastern Norwegian Sea. At the Arctic Front, the Arctic Intermediate water approaches the surface. Consequently, overwintering individuals may stay near-surface in the vicinity of the Arctic Front. Lower predation risk in the western Norwegian Sea compared with eastern region may facilitate higher survival of C. finmarchicus while staying in near-surface in this area (Dale et al., 1999). The seasonal cycle of C. finmarchicus seemed, independent of water masses and regions, to be related to the consumption of nitrate and hence to cumulative phytoplankton production. When the number of individuals of each copepodite stage was plotted against the consumption of nitrate, representing the phytoplankton development, the same events in the life cycle of C. finmarchicus were found at similar nitrate consumptions in different geographical areas in the Norwegian Sea (Fig. 4). This emphasizes the strong link between the phytoplankton bloom progression and the lifecycle of C. finmarchicus, and that the consumption of nitrate can be used as proxy for the phytoplankton seasonal development. Two generations of C. finmarchicus were found in the southern and northern regions of Coastal Water (although only the second generation was adequately covered by sampling in the north), and in southern Atlantic Water (Fig. 4). In northern Atlantic Water and in Arctic Water, one generation was observed. Temperature and food control growth and development. Higher temperatures and an earlier phytoplankton bloom in Coastal and southern Atlantic waters therefore may support two generations in these areas. Mixing of individuals from geographically adjacent areas must be expected, complicating the interpretation of the data. However, supporting the present study, previous investigations have suggested a 1-year lifecycle of C. finmarchicus in the northern and western part of the Norwegian Sea, while two or even more generations have been found in south and east (Wiborg, 1954; Østvedt, 1955; Matthews et al., 1978; Melle et al., 2004). We propose that a combination of delayed phytoplankton development and reduced sea water temperature make C. finmarchicus less successful in Arctic and northern waters of the Norwegian Sea. In the Norwegian Sea, spawning is linked to the phytoplankton pre-bloom and bloom, and thus occurs first in Coastal Water, later in Atlantic Water and latest in Arctic Water, and also from south to north within water masses. Low sea temperatures in northern Atlantic and Arctic regions coincide with additionally delayed development from eggs to CI and subsequent copepodite stages in these areas. C. finmarchicus therefore may not be able to accomplish their lifecycle within 1 year in Arctic and northern Norwegian Sea regions. C. glacialis and C. hyperboreus, which are adapted to multi-year life cycles (Tande et al., 1985; Hirche, 1997; Melle and Skjoldal, 1998) can postpone reproduction to subsequent years, while C. finmarchicus having only one proper overwintering stage with good fat storage capabilities, seems to require environmental conditions facilitating a 1-year life cycle. Consequently, C. finmarchicus is less successful in cold water areas with a delayed phytoplankton bloom. Present observation of very low numbers of young stages of C. finmarchicus overwintering in surface waters of cold regions supports this conclusion. A good understanding of the development of C. finmarchicus in the Norwegian Sea is important with respect to its key role as prey for large, seasonally migrating fish stocks. The migration pattern of Norwegian spring spawning herring may to a large extent be governed by the seasonal cycle of C. finmarchicus, due to stage specific predation of C. finmarchicus by herring (Østvedt, 1955; Melle et al., 1994; Dalpadado et al., 2000). The results of the present investigation will further be used to study the relation between C. finmarchicus and the Norwegian spring spawning herring in the Norwegian Sea. Acknowledgements We thank the Research Council of Norway for funding through the project /120 and /S30. We are grateful to Signe Johannessen and Bjørnar Ellertsen for help with analysing the