Distribution of Calanus Finmarchicus in the Northern North Atlantic and Arctic Ocean—Expatriation and Potential Colonization

ARTICLE IN PRESS

Deep-Sea Research II 54 (2007) 2729–2747 www.elsevier.com/locate/dsr2

Distribution of Calanus ﬁnmarchicus in the northern North Atlantic and Arctic Ocean—Expatriation and potential colonization

Hans-Ju¨ rgen Hirchea,Ã, Ksenia Kosobokovab

aAlfred Wegener Institute for Polar and Marine Research, Columbusstrasse 1, D-27568 Bremerhaven, Germany bP.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, 36 Nakhimov ave., Moscow 117997, Russia

Received in revised form 1 July 2007; accepted 10 August 2007 Available online 23 October 2007

Abstract

The distribution of Calanus finmarchicus was studied on a transect across the central Greenland Sea, and on five transects from the Eurasian shelves across the Atlantic Inflow in the Arctic Ocean. Stage composition was used as an indicator for successful growth; gonad maturity and egg production were taken as indicators for reproductive activity. On the Arctic Ocean transects, these parameters were measured simultaneously from the sibling species Calanus glacialis. Response of egg production rate to different temperatures at optimal food conditions was very similar between both species in the laboratory. C. finmarchicus was present at all stations studied, but young developmental stages were only present close to the regions of submergence of Atlantic water under the Polar water. This together with a decreasing abundance and biomass from west to east along the Atlantic Inflow in the Arctic Ocean and reproductive failure indicates that C. finmarchicus is expatriated in the Arctic Ocean. We hypothesize that the late availability of food in the Arctic Ocean, rather than low temperature per se, limits reproductive success. Better reproductive success in the very low temperature regions of the Return Atlantic Current and the marginal ice zone in the Greenland Sea supports this hypothesis. The possibility for a replacement of C. glacialis by C. finmarchicus and consequences for the ecosystem after increasing warming of the Arctic are discussed. r 2007 Elsevier Ltd. All rights reserved.

Keywords: Calanus ﬁnmarchicus; Calanus glacialis; Expatriation; Climate change; Arctic Ocean

1. Introduction Conover, 1988). Its centre of activity is confined to ice-free water, while its congeners, Calanus hyper- Calanus finmarchicus is a key species in the boreus and Calanus glacialis, inhabit the seasonal zooplankton of the North Atlantic, where it is prey ice-covered seas and the Arctic Ocean (Conover, for many species of fish. Due to its biomass, its role 1988). Due to the circulation system in the North in carbon flux is also important. C. finmarchicus is Atlantic, high numbers of C. finmarchicus are found all over the North Atlantic (Jaschnov, 1970; transported by the North Atlantic Current (NAC) into subarctic and arctic seas. The main northward ÃCorresponding author. Fax: +49 471 4831 1918. transport of Atlantic water is through the NAC and E-mail address: [email protected] (H.-J. Hirche). its northern continuation, the West Spitsbergen

Current (WSC), which, after its passage through the maturation in adult females. On the other hand, Greenland Sea, finally drains into the Arctic Ocean females collected in the EGC in June at 1.6 1C in Fram Strait. In the Greenland Sea, part of the continued to spawn at 0 1C for 22 days (end of Atlantic water recirculates and flows southwards as experiment), and females collected in the WSC in the Return Atlantic Current (RAC) along the East April spawned continuously for 77 days at 0 1C Greenland Shelf (EGS) underneath the Polar waters (Hirche, 1990). of the East Greenland Current (EGC) (Gascard Recent climate models forecast large environ- et al., 1988). Via troughs, Atlantic water also mental changes, especially in the subarctic and reaches far onto the EGS (Bude´ us and Schneider, arctic regions (Polyakov et al., 2002). These changes 1995). The large frontal systems of the Arctic Front include increase of water temperatures, thinning of (AF) in the east and the East Greenland Polar Front sea ice, and reduction of the duration of ice (EGPF) in the west are interfaces between Atlantic, coverage (Johannessen et al., 2002). Increased Arctic and Polar water masses and allow exchange inflow of Atlantic water into the Arctic Ocean has of faunistic elements. Atlantic water is advected been observed, which caused a shift in the balance onto the Barents Shelf from the Lofoten Basin between Pacific and Atlantic waters there (Carmack through the Barents Sea Opening into the Barents et al., 1995; McLaughlin et al., 1996, 2002; Swift Sea (Loeng, 1991). Portions of Atlantic water et al., 1997). Although we do not know yet which submerge under the lighter Arctic water at the physiological or other barriers prevent C. finmarch- Polar Front and flow north following troughs on icus from inhabiting these regions, it is possible that the shelf (Schauer et al., 2002). From the north, the environmental changes associated with the branches of Atlantic water enter the Barents Sea climate changes will allow future colonization between Nordaustlandet and Franz-Josef-Land as a and replacement of the autochthonous congeners near-bottom water mass (Pfirman et al., 1994). C. glacialis and C. hyperboreus. This would drama- In the Arctic Ocean, water of Atlantic origin tically affect the ecosystems, as C. finmarchicus is forms a layer several 100 m thick between 200 and smaller and has a different life cycle strategy than 1000 m depth. Atlantic water enters mainly via the the other species. Fram Strait (Rudels et al., 1994) and forms a Here we describe the distribution of C. finmarch- boundary current running counter-clockwise along icus on transects across the central Greenland Sea the perimeter of the Arctic Ocean. Recirculating and the Atlantic Inflow in the Arctic Ocean branches of Atlantic water are deflected seaward combining observations from several expeditions. where mid-ocean ridges, like the Nansen-Gakkel By comparing total abundance with stage composi- Ridge, the Lomonosov Ridge (Anderson et al., tion (as an indicator for active growth), and with 1989), and the Alpha-Mendeleev Ridge, meet the gonad stage and egg production rate (as indicators Eurasian Shelf (Rudels et al., 1994). of reproductive activity) on transects across differ- While in many of these regions C. finmarchicus ent water masses, we try to distinguish expatriated constitutes a large part of the biomass (Hirche and populations from actively growing and reproducing Mumm, 1992; Kosobokova and Hirche, 2000), we ones. As reduced growth and reproduction of suggest that it is not actively growing and reprodu- C. finmarchicus could instead be caused by food cing there, but is expatriated. The low temperatures limitation, we used the sibling species C. glacialis as in Polar water have been suggested as the cause for an indicator for feeding conditions, assuming that low growth and reproduction of C. finmarchicus in food requirements and preferences are similar. the Arctic Ocean (Jaschnov, 1970). Corkett et al. Finally, we compared egg production rates of the (1986) observed embryonic development at 0 1C, two species at different temperatures in the labora- development to CI at 2 1C, and older stages at 5 1C, tory and in the field. but do not comment why they did not conduct all measurements at 0 1C. Campbell et al. (2001) for C. 2. Material and methods finmarchicus and Thompson (1982) for Calanus spp. studied the development at 4, 8, and 12 1C and 2.1. Zooplankton collection found successful growth at all temperatures. Tande et al. (1985) and Hansen et al. (1996) assumed from Calanus spp. were collected during several field observations in the Barents Sea that tempera- expeditions of the RV ‘Polarstern’ to the Greenland ture hindered gonad development of CV and ovary Sea and the Arctic Ocean. Cruise dates and station ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2731 locations are listed in Table 1, transects and station 2.2. Taxonomy and prosome length positions are shown in Fig. 1. On transect GS (Fig. 1) zooplankton was collected with vertical For differentiation between C. finmarchicus and tows by a bongo net (310 mm mesh) in the upper C. glacialis, prosome length established by Hirche 80 m. On transect BS it was collected with a bongo et al. (1994) in the Greenland Sea was used (Table 2). net (310 mm mesh) in the upper 100 m and with a The prosome length of at least 60 individuals of Multi-net (Hydrobios, Kiel, 0.25 m2 mouth opening, each stage was measured with a micrometer at 25 150 mm mesh) in five depth strata down to the magnification to the nearest 0.04 mm between the bottom (Table 1). At transects W, E, F five strata tip of the cephalosome and the end of the last down to 1500 m or to the bottom were sampled, at thoracic segment. As prosome length, among other transects B and H from five to nine depth layers factors, is controlled by the temperature during were sampled down to the bottom with the same development, different body sizes are found for the model of Multi-net. Samples were preserved in 4% same species in different regions. As prosome borax–buffered formaldehyde. All copepodite lengths often overlap between species, this criterion stages of the two species were counted in the is not absolutely reliable. Especially when one samples. species is represented by a very small fraction, the

Table 1 Sampling locations, bottom depth and maximum sampling depth (m)

Cruise Transect, Latitude, N Longitude Date Bottom Maximum depth Egg production station no. depth, (m) of haul (m) experiments

ARK VI/3 Transect GS 66 74130 14130W 11 June 89 250 80 Pooled 67 74135 14100 11 June 89 400 80 Pooled 68 74142 13130 11 June 89 518 80 Pooled 69 74145 131 11 June 89 770 80 Pooled 70 74145 12120 11 June 89 2150 80 Pooled 71 741145 11140 12 June 89 2700 80 Pooled 72 74145 11100 12 June 89 3050 80 Pooled 73 74145 10125 12 June 89 3190 80 Pooled 74 74145 9145 12 June 89 3270 80 Pooled 76 74145 8130 13 June 89 3345 80 Pooled 78 74145 7117 13 June 89 3450 80 Pooled 80 74145 6100 13 June 89 3524 80 Pooled 82 74145 4144 13 June 89 3600 80 Pooled 84 74145 3138 14 June 89 3655 80 Pooled 86 74145 2113W 14 June 89 3680 80 Pooled 88 74145 0157W 14 June 89 3400 80 Pooled 91 74145 1102E 15 June 89 3770 80 Pooled 93 74145 2113 15 June 89 3771 80 Pooled 95 74145 3128 15 June 89 3314 80 Pooled 97 74145 4146 16 June 89 3450 80 Pooled 99 74145 6103 16 June 89 2980 80 Pooled 100 74145 6140 16 June 89 2250 80 Pooled 101 74145 7115 16 June 89 2130 80 Pooled 102 74145 7155 16 June 89 2430 80 Pooled 103 74145 8135 17 June 89 3250 80 Pooled 104 74145 9112 17 June 89 2580 80 Pooled 105 74145 9150 17 June 89 2585 80 Pooled 106 74145 10129 17 June 89 2515 80 Pooled 107 74145 11105 17 June 89 2490 80 Pooled 108 74145 11145 17 June 89 2448 80 Pooled 110 74145 13100 18 June 89 2250 80 Pooled 112 74145 14115 18 June 89 1950 80 Pooled 114 74145 15132E 18 June 89 820 80 Pooled ARTICLE IN PRESS 2732 H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747

Table 1 (continued )

Cruise Transect, Latitude, N Longitude Date Bottom Maximum depth Egg production station no. depth, (m) of haul (m) experiments

ARK IX/4 Transect W 6811120 301360E 12 Aug 93 188 160 Single and pooled 7811280 301530 13 Aug 93 525 490 Single and pooled 14 811400 301160 13 Aug 93 2701 1500 Single and pooled 19 821120 341300 15 Aug 93 2456 1500 Single and pooled ARK IX/4 Transect F 32 781430 1321210 2 Sep 93 2987 1500 Single and pooled 35 781230 1331040 4 Sep 93 2062 1500 Single and pooled 38 781100 1331230 5 Sep 93 982 950 Single and pooled 39 781060 1331340 5 Sep 93 446 450 Single and pooled ARK IX/4 Transect E 54 791110 1191540 13 Sep 93 3067 1500 Single and pooled 56 781400 1181430 14 Sep 93 2615 1500 Single and pooled 58 781000 1181330 15 Sep 93 1930 1500 Single and pooled 60 771330 1181260 16 Sep 93 1178 1000 Single and pooled 62 771240 1181110 17 Sep 93 556 500 Single and pooled

ARK XI/1 Transect B 25 811060 1051230E 7 Aug 95 2642 2500 Single and pooled 27 811140 1061450 8 Aug 95 3133 3000 Single and pooled 31 801460 1031230 11 Aug 95 1435 1400 Single and pooled 32 801390 1031030 11 Aug 95 621 500 Single and pooled 33 801250 1011590 12 Aug 95 266 245 Single and pooled ARK XI/1 Transect H 75 801550 1221400 4 Sep 95 3566 3500 Single and pooled 47 801550 1321000 20 Aug 95 3907 3500 Single and pooled 49 811030 1361320 22 Aug 95 2708 2600 Single and pooled 51a 811070 1381470 23 Aug 95 1830 1700 Single and pooled 52 811100 1401060 24 Aug 95 1292 1200 Single and pooled 55 811110 1431240 25 Aug 95 1693 1600 Single and pooled 57 811120 1501150 27 Aug 95 2643 2500 Single and pooled

MN ¼ multi-net, Bo ¼ bongo net. Egg production experiments: single ¼ single females in 250 mL, pooled ¼ 20–30 females in 3 L beakers. overlapping tails of the length frequency distribu- Kosobokova (1999) were adapted to distinguish tion lead to a substantial over-estimation of the the following five states of gonad maturation: smaller fraction (Unstad and Tande, 1991). I. Immature: ovary compact, no oocytes in diver- 2.3. Dry mass ticulae and oviducts. II. Semi-mature: one or several rows of small Dry mass was calculated using dry mass size immature oocytes in diverticulae and oviducts. coefficients of copepodids and adults of C. finmar- III. Mature: several rows of immature oocytes chicus and C. glacialis from Hirche and Kosobokova densely packed into diverticulae; pouches of (2003, see their Table 2). oocytes in oviducts; ventral row of oocytes in diverticulae and oviducts formed by large 2.4. Gonad maturation stages mature oocytes. IV. Semi-spent: few small oocytes in the ovary, Gonad maturation of preserved females used in single oocytes spread irregularly in diverticulae egg production experiments was examined under a and oviducts. stereo microscope. Females were stained with borax V. Spent: diverticulae and oviducts as thin bands; carmine (2%) in ethanol (70%). The criteria given in no oocytes in the ovary; posterior of ovary Smith (1990), Niehoff and Hirche (1996) and extends to the third thoracic segment. ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2733

Fig. 1. Circulation of Atlantic water in the northern North Atlantic with location of stations (ﬁrst and last station number indicated) and transects used in this study. White arrow ¼ AW on the surface; black arrow ¼ submerged ﬂow of AW. Hatched area in inserted map ¼ marginal ice zone (MIZ). RAC ¼ Return Atlantic Current, WSC ¼ West Spitsbergen Current.

2.5. Egg production experiments (150 mL) having mesh (330 mm) false bottoms to separate eggs from females. Cylinders were then Females for in-situ egg production experiments suspended in 250-mL beakers with surface pre- were collected with bongo hauls (0.6 m diameter, screened (100 mm) seawater at ambient temperature 310 mm mesh) in the upper 80 or 100 m. Females (mean of water column sampled). On other cruises, were sorted immediately after collection. Single between 20 and 30 females were pooled and females were incubated in plexiglass cylinders incubated in 3-L beakers. Incubation methods used ARTICLE IN PRESS 2734 H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747

Table 2 Prosome lengths (mm) from the literature and values used to distinguish copepodids and adult female Calanus ﬁnmarchicus and C. glacialis in this study

C. ﬁnmarchicus C. glacialis

Stage Tande et al. Unstad and Hirche et al. Kosteyn and Hirche et al. (1985) Tande (1991) (1994) Kwasniewski (1992) (1994)

CI o0.85 o0.82 0.84–1.04 40.82 CII o1.2 o1.24 1.20–1.45 41.24 CIII o1.65 o1.6 1.70–2.05 41.6 CIV o2.3 o2.2 2.35–2.80 42.2 CV 2.5–2.9 o3.0 o3.0 3.05–3.95 43.0 AF 2.7–3.1 o3.2 o3.2 3.50–4.40 43.2 during the different cruises are included in Table 1. were log or log(1+x) transformed where necessary For long-term incubations to study the effect of to obtain normality and to homogenize variances temperature on egg production, 8–16 females were (Zar, 1996). More than one independent variable fed cultures of Thalassiosira antarctica grown on f/4 were only included in the model if they led to a more medium at concentrations 4400 mmCL1 for than 20% increase in the adjusted R2. The adjusted 10–16 days at 0 1C. Thereafter, single females were R2 is a modification of R2 that adjusts for the transferred to containers as described above and number of explanatory terms in the model. Unlike exposed to temperatures between 1.8 and 8 1C for R2, the adjusted R2 increases only if the new a period of 15 days. Egg production at each independent variable improves the model more temperature was calculated as the mean of all days than would be expected by chance (Zar, 1996). at a given temperature except the first 2 days after Statistical analyses were performed at a ¼ 0.05 with start of the experiment. In C. finmarchicus this delay STATISTICA 6.1 (StatSoft Inc.). is required to adjust egg production to the new temperature (Hirche et al., 1997). Light was 3. Results provided continuously by a daylight fluorescent bulb at 4 mEm2. After 24 h, cylinders were 3.1. Central Greenland Sea—Transect GS transferred to new containers with fresh food, and eggs were counted. Our transect crossed the central Greenland Sea from the EGS to the foot of the Barents Shelf near 2.6. Chlorophyll Bear Island, and thus included the three hydrographic domains of the Greenland Sea: the Polar Samples for the determination of chlorophyll-a domain on the EGS, the Arctic domain of the were taken from a Rosette sampling system in steps Greenland Sea Gyre (GSG), and the Atlantic of 10 m from the surface to 50 m. Concentrations of domain of the WSC. Topography and distribution chlorophyll-a and phaeopigments were determined of the potential temperature across our transect is on a Turner Designs fluorometer after grinding and shown in Bude´ us et al. (1993), the general hydro- extracting (90% acetone) filters (GF/C) from water graphy of the Greenland Sea has been described in casts. For calibration, pure chlorophyll-a in 90% detail by Meincke et al. (1992) and Bude´ us et al. acetone (Sigma) was used. (1993). In the ice covered Polar Domain (stations 66–69) temperatures were close to the freezing point 2.7. Statistics down to about 40 m depth. The Polar waters were confined to relatively shallow depths as they were C. finmarchicus egg production rates, water underlain by Atlantic influenced waters from 150 m temperature and chlorophyll-a concentration were downwards. Therefore the EGPF at stations 69/70 tested for correlation using non-parametric Spear- did not reach to the bottom. The RAC flowing man’s correlation analysis. Then, multiple regression southward under Polar water at stations 69–73 had analysis was conducted using C. finmarchicus egg maximum temperatures of up to 2 1C (station 69) in production rates as dependent variable. Variables its core at 150 m. In the central basin, temperatures ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2735 in the upper 80 m ranged from 0.75 to 0.5 1C. At ranging from 0.1 to 13.3. In the frontal area of the the AF (stations 101/102), which separates the AF (stations 99–101), at temperatures from 0.5 to Arctic from the Atlantic domain, the temperature 1.5 1C, mean egg production rate was 4.8 (range as well as the salinity front extended almost 4.6–5.0). In the GSG there were not sufficient vertically to the surface in the upper 200 m between females to set up experiments. At stations 69–71, stations 99 and 102. Between 200 and 300 m depth, located on top of the RAC, C. finmarchicus a warm and saline westward intrusion indicated produced between 0.2 and 2.6 eggs female1 d1, some cross frontal exchange. Temperatures in the respectively. On the EGS no eggs were produced by upper 80 m of the WSC were between 4 and 6.5 1C. C. finmarchicus, but C. glacialis laid 2 and 1.5 eggs Transect GS shows high concentrations of C. finmar- female1 d1 at stations 67 and 68, respectively. chicus in the WSC east of the AF (Fig. 2). The elevated concentrations in the west at stations 69–72 (EGPF) 3.2. Marginal ice zone (MIZ) of the Greenland are clearly associated with the RAC. Fig. 2 shows Sea—MIZ also, that C. finmarchicus is present in the central GSG and on the EGS, however, at much lower The hydrography of the MIZ in the Fram Strait concentrations. Only the stages CIV to CVI were during our study has been described in detail by distinguished, but their ratios varied between the Johannessen et al. (1987), Manley (1987) and different water masses: 11.576.7% (CIV), 53.97 Gascard et al. (1988); the zooplankton dynamics 9.0% (CV) and 34.679.3% (females) in the WSC; by Smith et al. (1985), Smith (1987),andHirche 35.578.4%, 48.679.3%, and 15.977.0% in the (2004). The position of the MIZ in the Greenland GSG; and 29.471.6%, 53.775.5%, and 16.87 Sea is mainly controlled by the position of the 3.9% on the EGS, respectively. EGPF (Bourke et al., 1988) and therefore relatively Egg production was measured at 17 stations with invariant in space in contrast to the MIZ in other C. finmarchicus and two stations with both C. regions, where a receding ice edge in summer is finmarchicus and C. glacialis (Fig. 3A). In the WSC, followed by ice-edge blooms. The position of the ice mean egg production was 4.3 eggs female1 d1, edge in 1984 changed rapidly during the cruise due

600 WSC AF CV 500 CIV

) 400 -3

RAC 300 EGC GSG

Abundance (n m 200

100

0 66 67 68 69 70 71 72 73 74 76 78 80 82 84 86 88 91 93 95 97 99 100 101 102 103 104 105 106 107 108 110 112 114 Station

Fig. 2. Distribution of copepodids CIV, CV and adult females of Calanus ﬁnmarchicus across the central Greenland Sea (741450N). EGC ¼ East Greenland Current, RAC ¼ Return Atlantic Current, GSG ¼ Greenland Sea Gyre, WSC ¼ West Spitsbergen Current. ARTICLE IN PRESS 2736 H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747

100 (A) C.finmarchicus

) Greenland Sea C.glacialis -1 Barents Sea C.finmarchicus d

-1 80 C.glacialis

20 Egg production rate (eggs female

0 -2 -1 0 1 2 3 4 5 6 7 8 9 80 (B) C.finmarchicus Chl a ) -1 d -1 60 ) -2 (mg m a 40 Chlorophyll 20 Egg production rate (eggs female

0 -2 -1 0 1 2 3 4 5 6 7 8 9 Temperature (°C)

Fig. 3. Egg production (eggs female1 d1)ofCalanus finmarchicus in relation to temperature in the upper 80 m (A) on Transect GS across the central Greenland Sea and on Transect BS in the Barents Sea; (B) in the Marginal Ice Zone of the Greenland Sea (MIZ in Fig. 1). Solid line ¼ egg production rate of C. finmarchicus at optimum food conditions (see Fig. 8). to changes in winds and currents. In addition, stations in the MIZ (Fig. 1) and plotted against the various eddies shaped its appearance by their own mean seawater temperature in the upper 80 m, drift and by advecting ice into the open water. where females were collected (Fig. 3B). Females A study by Smith et al. (1985) in the MIZ of the were laying eggs at temperatures down to o1 1C. Greenland Sea found C. finmarchicus present in the A comparison with the experimental egg production three neighbouring water masses. It dominated rates at maximum food concentrations from Hirche waters of Atlantic origin and was represented by et al. (1997) shows that C. finmarchicus females were all copepodite stages, while in Arctic and Polar always food limited (Fig. 2C). C. finmarchicus egg waters mostly CV and females were found, similar production rates, seawater temperature and chlor- to the western part of Transect GSG. During the ophyll-a concentration were all positively correlated same study, egg production was measured at 71 with each other. multiple linear regression analysis ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2737 showed that the best prediction of egg production Station 19 was to the north of the Atlantic Inflow rates was obtained with a model using log (x+1) and dominated by Arctic water. egg production rates as dependent variable and log A large percentages of young stages of both chlorophyll-a concentration and water temperature C. finmarchicus and C. glacialis were found at the as independent variables. Adjusted R2 using both southern end of the transect (especially at station 7 variables was 0.48, clearly better than the adjusted on the shelf break), while older stages dominated R2 of 0.38 and 0.33 obtained for simple linear the deep stations (Fig. 4). Pronounced maxima of regression models using only water temperature and both abundance and biomass of C. finmarchicus log chlorophyll-a as independent variables, respec- were centred on the shelf break (sta. 7, Fig. 5). By tively. Regression slopes were significantly different far the majority were in the upper 100 m, but at the from zero in both simple linear regression models deep stations 14 and 16 a few specimens were also and for the multiple linear regression model found in the deepest samples (Fig. 6). On a transect (po0.0001, unadjusted overall R2 ¼ 0.50, n ¼ 46). in 1987, which started at a similar location but extended at the Nansen-Gakkel Ridge, Hirche and Mumm (1992) found C. finmarchicus dominated the 3.3. Barents Sea—Transect BS mesozooplankton biomass in the Atlantic Inflow, but noted a drastic drop in abundance and almost Two meridional transects along 331E across the complete disappearance of younger stages asso- Polar Front of the northern Barents Sea (Fig. 1)in ciated with an abrupt change in water masses at ca. May and June 1997 have been published before and 831N(Anderson et al., 1989). are here summarized for completeness (Hirche C. finmarchicus laid few eggs (range 0.41–3.25) at and Kosobokova, 2003). All copepodite stages of three of four stations, while C. glacialis spawned C. finmarchicus were found south of the front in between 16 and 22 eggs female1 d1 at the two Atlantic water, but stages CI and CII were rare in stations where experiments were set up (Fig. 7). the Polar domain north of the front. Egg produc- Gonad maturation data were consistent with these tion rates, the portion of spawning females, and results. Between 14% and 26% of the C. finmarch- young copepodids were much higher in C. glacialis icus females were mature, whereas in C. glacialis, than in C. finmarchicus in the Polar domain close to except for station 7, more than half of the females the front, while farther to the north, insufficient were mature (Fig. 7). In the study by Hirche and female C. finmarchicus were found to set up Mumm (1992, their Tables 2 and 3) C. finmar- experiments. It is worthwhile mentioning, however, chicus produced eggs at only one station in the that C. finmarchicus had relatively high egg produc- Atlantic Inflow water (0.3 eggs female1 d1), while tion rates at temperatures around 1 1C, when C. glacialis spawned at four stations. After feeding compared with individuals obtained on the Green- females of the two species with superabundant food land Sea Transect (Fig. 3A). Results of incubation for 11 days, C. glacialis laid slightly more eggs. At experiments were supported by a tremendous the one station where such experiments were also abundance of C. glacialis eggs in the water column. conducted with C. finmarchicus, egg production also In contrast, no eggs of C. finmarchicus were found increased from 0.3 to 1 eggs female1 d1. in the Polar domain 430 nm north of the front. 3.5. Arctic Ocean—Transect B 3.4. Arctic Ocean—Transect W Hydrography for Transect B covering five sta- Hydrography for Transect W covering four tions from the Laptev Sea Shelf to the eastern stations from the Barents Shelf to the Western Nansen Basin in 1995 was described by Rudels et al. Nansen Basin in 1993 was described by Schauer (2000, their Transect B). A cold, low-salinity water et al. (1997, their Transect I). Under a layer of cold, column over the shelf and slope reaching down to low-salinity Arctic Surface water of ca. 100 m more than 1000 m, the Barents Sea branch of the thickness, a relatively cold, low salinity layer of Atlantic Inflow, was separated by a 40-km wide Northern Barents Sea Water was situated on the frontal zone from a warm (almost 3 1C), high- slope between stations 6 and 7, and was replaced by salinity core located at 300 m depth in the basin at warm (43 1C at 200 m) Atlantic water 30–40 km the northern side of the transect, the Fram Strait seaward of the shelf break (stations 7 and 14). branch. ARTICLE IN PRESS 2738 H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747

C. finmarchicus C. glacialis 100% 80 60 40 20 0 6 7 14 16 6 7 14 16

100% 80 60 B 40 20 0 33 32 31 25 27 33 32 31 25 27

100% 80 60 40 20 0 62 60 58 56 54 62 60 58 56 54

100% 80 60 F 40 20 0 39 38 35 32 39 38 35 32

100% 80 60 HEW 40 20 0 47 49 51a 52 55 57 47 49 51a 52 55 57 Station No. CI CIII CV

CII CIV Fem

Fig. 4. Stage composition of Calanus ﬁnmarchicus and C. glacialis on transects (from south to north) across the Atlantic Inﬂow in the Arctic Ocean (for station and transect locations see Fig. 1 and Table 1).

C. ﬁnmarchicus was almost exclusively repre- at all stations except the deepest (sta. 27, Fig. 4). sented by CV (ca. 70%) and females (ca. 30%). Abundance of C. ﬁnmarchicus was much lower than Young stages of C. glacialis (mostly CI), dominated on Transect W and was more or less constant across ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2739

20000 3.6. Arctic Ocean—Transect E (A) 18000 16000 Hydrography for Transect E covering five sta- 14000 tions from the Laptev shelf break to the western Transects Nansen Basin in 1993 also was described by Schauer 12000 W 10000 B et al. (1997, their Transect III). The Atlantic Inflow E 8000 F located below 200 m extended from station 58–54 6000 under a layer of cold, low-salinity Arctic Surface Calanus glacialis 4000 water of ca. 150 m thickness. 2000 As in the previous Transect B, both C. finmarchicus and C. glacialis were mainly represented by CV 0 0 1000 2000 3000 (ca. 65%) and females (ca. 35%) (Fig. 4). Only 20000 few younger stages were observed, mainly CIII (B) 30648 18000 (ca. 10%). Abundance of C. finmarchicus was much 16000 lower than on the upstream Transect W (Fig. 5).

-2 14000 Transects Vertical distribution was restricted to the upper W 12000 B 200 m, and at most stations maximum abundance E was in the 25–50-m sample (Fig. 6). 10000 F Neither C. finmarchicus nor C. glacialis produced 8000 any eggs, probably due to severe ice conditions in 6000 Abundance nm this region (Kosobokova and Hirche, 2001, their Calanusfinmarchicus 4000 Transect F). 2000 0 0 1000 2000 3000 Bottom depth (m) 3.7. Arctic Ocean—Transect F 4000 (C) C. finmarchicus Hydrography for Transect F covering four C. glacialis Transect H stations from the Laptev shelf break to the 3000 Amundsen Basin (AB) in 1993 was also described LR by Schauer et al. (1997, their Transect V). Under a layer of cold, low-salinity Arctic Surface water of 2000 ca. 100 m thickness the warm Atlantic water was NGR MB found all along the transect. This transect crossed the Laptev Sea polynya in the eastern Laptev Sea. 1000 AB In summer 1993, the region extending northward from the mouth of the river Lena was already 0 open by early August and relatively high chlor- 75 47 49 51a 52 55 57 ophyll concentrations were found at stations 38–40 Station (Kosobokova and Hirche, 2001). Fig. 5. Abundance of Calanus finmarchicus (A) and C. glacialis The distribution of C. finmarchicus was similar to (B) on Transects W,B,E,F, and of both species (C) on Transect H Transect E. The population consisted almost across the Atlantic Inflow in the Arctic Ocean (for station and exclusively of CV and adult females, the latter made transect locations see Fig. 1 and Table 1). NGR ¼ Nansen- up 50% of all stages at station 38. In addition at the Gakkel-Ridge, AB ¼ Amundsen Basin, LR ¼ Lomonosov- Ridge, MB ¼ Makarov Basin. shelf break a number of CIV were present (Fig. 4). In contrast, the C. glacialis population was characterized by a large portion of younger stages on the shallow stations, which decreased towards the the whole transect (Fig. 5). C. finmarchicus was deeper basin (Fig. 4). Abundance and biomass of present only in the upper 250 m; abundance was at a C. finmarchicus were almost identical to Transect E maximum in the 25–50 m layer; at the deepest (Fig. 5). Vertical distribution was shallower than on station 27 there was a second maximum in the Transect E, with the vast majority of specimens in 100–200 m layer (Fig. 6). the upper 50 m (Fig. 6). ARTICLE IN PRESS 2740 H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747

Abundance, ind m-3 0 50 100 150 010203040 010155 0 0 0

200 200 200

400 400 400

600 600 600 Transect W Transect B Transect E Sta 6 Sta 33 Sta 62 800 800 800 Sta 7 Sta 32 Depth, m Sta 60 Sta 31 Sta 16 Sta 58 1000 Sta 25 1000 Sta 14 1000 Sta 54 Sta 27

1200 1200 1200

1400 1400 1400

0101520255550101501015 0 0 0

200 200 200

400 400 400

600 600 600 Transect F Transect H Transect H Sta 75 Sta 55 Sta 39 800 800 800 Sta 47 Sta 57

Depth, m Sta 38 Sta 49 Sta 52 Sta 35 1000 1000 1000 Sta 51 Sta 32

1200 1200 1200

1400 1400 1400

Fig. 6. Vertical distribution of Calanus ﬁnmarchicus on transects across the Atlantic Inﬂow in the Arctic Ocean (for station and transect locations see Fig. 1 and Table 1).

In Fig. 7 gonad stage and egg production rates during experiments at five stations. In contrast, on Transect F are compared for C. finmarchicus and young copepodids of C. glacialis were present at C. glacialis (C. glacialis from Kosobokova and four stations on the slope near the ice edge Hirche, 2001, their Transect H). Between 62% (Kosobokova et al., 1998, their Table 6). Females and 92% of the C. finmarchicus females were spent produced up to 8 eggs female1 d1 at four stations, or showed signs of resorption, the rest of the in most females gonads were spent, with up to 30% females were immature. No eggs were produced immature. ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2741

spent semi-spent ripe semi-ripe immature Transect W Transect F EPR 3.3 0.4 0 1.0 -- 0 -- 000 0 0 100

20 Gonad maturity (%) Calanus finmarchicus 0

EPR 22.3-- 15.7 --3.1 -- 0 2.6 2.5 8.30.1 0 100

20 Calanus glacialis Gonad maturity (%) 0 Station 6 67 14 19 31 43 41 40 39 38 35 32 Depth (m) 180 490 2720 2994 38 53 72 243 513 982 2062 2975

Fig. 7. Gonad maturation stages and egg production rates (EPR) (eggs female1 d1)ofCalanus ﬁnmarchicus and C. glacialis on Transects W and F across the Atlantic Inﬂow in the Arctic Ocean (see Fig. 1). Data for C. glacialis from Kosobokova and Hirche, 1991).

3.8. Arctic Ocean—Transect H transects (Fig. 5). This is in good agreement with hydrographic observations that near the Laptev Hydrography and ice cover during Transect H shelf about half of the Atlantic Inflow flow is from the AB across the Lomonosov Ridge to the diverted north along the Eurasian Basin side of the Makarov Basin (MB) were described in detail by Lomonosov Ridge (Woodgate et al., 2001). As on Rudels et al. (2000, part of their Transect C) and all other transects, C. finmarchicus were concen- summarized by Kosobokova and Hirche (2000). trated in the upper 100 m with the maximum The core of the Atlantic water flows to the north on abundance in the 20–50-m layer. At some stations the Eurasian side of the Lomonosov Ridge (stations a secondary maximum was observed between 100 51a, 52). Two branches of Atlantic water from the and 200 m (Fig. 6). Norwegian Sea were identified by salinity maxima, Although egg production experiments were set up representing the Barents Sea branch and the Fram at all stations, neither C. finmarchicus nor C. glacialis Strait branch. The Atlantic water probably crosses spawned any eggs. the ridge at various latitudes south of 86.51N and flows southward along the MB side of the ridge (Woodgate et al., 2001). 4. Temperature and reproduction—laboratory While all copepodite stages of C. glacialis were studies present at almost all stations, C. finmarchicus was almost exclusively represented as CV and adults in In egg production experiments, C. finmarchicus almost equal proportion (Fig. 4). Highest concen- collected in the northern Norwegian Sea at 9 1C trations of both species were observed on the crest were incubated at five temperatures after acclima- of the Lomonosov Ridge (stations 51a, 52), where tion at 0 1C for 4–7 days (Hirche et al., 1997). They the core of Atlantic water was located. Abundance laid eggs in regular intervals during ca. 2 weeks. of C. finmarchicus on this transect ranged from 204 Egg production rate increased exponentially with to 830 individuals m2 and was the lowest of all temperature over the range between 1.5 and 8 1C. ARTICLE IN PRESS 2742 H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 )

-1 80 water, including its fauna, submerges under the d C.glacialis R2 = 0.979 -1 Polar water below ca. 100 m. (3) While in the C.finmarchicus R2 = 0.976 northern Barents Sea Atlantic water submerges over 60 a wide area, the RAC and Atlantic Inflow form relatively narrow submerged bands of flow travel- ling long distances from their origin in the Fram 40 Strait (Bourke et al., 1988; Woodgate et al., 2001). C. finmarchicus preferred the surface or near-surface layer, despite the fact that the submerged Atlantic 20 water is covered by a layer of cold Polar water often more than 200 m in thickness. At most stations, the vertical distribution maximum was between 25 and 0 Egg production rate (eggs female -2 -1 0 1 2 3 4 5 6 7 8 9 50 m. In addition, at some stations a second Temperature (°C) maximum was found between 100 and 200 m. In contrast, in the Atlantic layer between 200 and Fig. 8. Egg production rates of Calanus finmarchicus and 900 m, hardly any C. finmarchicus were observed C. glacialis at different temperatures and optimum food concen- (Fig. 6). Similarly, in the northern Barents Sea trations (data for C. finmarchicus from Hirche et al., 1997), (vertical bars7st.dev.). C. finmarchicus was found in the upper layers directly north of the front, indicating an immediate The temperature response of C. glacialis treated ascent after submergence of the Atlantic water equally in the experiments was very similar (Fig. 8). (Hirche and Kosobokova, 2003). This vertical distribution should have strong consequences for the advection of C. finmarchicus, as the submerged 5. Discussion Atlantic water and the surface layer often flow in different directions (Woodgate et al., 2001). 5.1. Distribution and hydrography Although for the Arctic Ocean no data on the vertical distribution in winter are available, we During this study C. finmarchicus was observed at assume, based on observations from the Greenland all stations studied in the Greenland Sea, the Sea (Hirche, 1991) and Norwegian Sea (Østvedt, Barents Sea, in the Eurasian Basins, and the MB 1955), that C. finmarchicus performs seasonal in the Arctic Ocean. Including published informa- migrations and spends most of its life in deeper tion on Davis Strait (Huntley et al., 1983) and waters, where it is then advected along with the Baffin Bay (Ringuette et al., 2000), we can general- Atlantic Inflow farther into the Arctic Ocean. ize that the species is found all over the North Furthermore, we assume that overwintering stages Atlantic and the eastern Arctic Ocean (Jaschnov, maintain their depth when Atlantic water sub- 1970; Conover, 1988) in close association with the merges. As a consequence, the speed and direction flow of Atlantic water. This makes the species a of advection of C. finmarchicus in all areas of good tracer, as suggested earlier by Jaschnov (1970). submergence of Atlantic water should underlie Depending on the depth distribution and flow seasonal variations. pattern of the Atlantic water, three different expatriation patterns are possible. (1) On transect 5.2. Expatriation and factors controlling recruitment GS across the AF in the Greenland Sea, Atlantic and Arctic water masses are aligned in the upper Our observations on stage composition, abun- layer. The biomass of C. finmarchicus decreased by a dance and reproductive activity clearly suggest that factor 10 within 10 nm of the frontal zone indicating C. finmarchicus is not recruiting successfully in the little cross-frontal exchange, despite the numerous northern Barents Sea nor in the Arctic Ocean. eddies in this there (Trees et al., 1992; Walczowski Young developmental stages were only present near and Maslowski, 2003) that could accelerate cross- the source regions, as on Transect W shortly past frontal exchange processes. (2) On Transect BS the entrance to the Arctic Ocean, and on Transect across the Polar Front of the Barents Sea (Hirche BS just north of the Polar Front (Hirche and and Kosobokova, 2003) Atlantic and Polar waters Kosobokova, 2003), where they were probably are also aligned in the upper layer, but Atlantic advected only recently. Furthermore, a downstream ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2743 decrease of abundance and biomass along the in late summer entered the Arctic Ocean during the Atlantic Inflow and across the Lomonossov Ridge previous fall and winter as CV, as this stage is by far was observed for consecutive transects during the the dominant over wintering stage in the Greenland same years (1995: B, H; 1997: W, E, F). Gonad Sea (Hirche, 1991). This assumption is based on stages and egg production measurements further mooring data near the Lomonossov Ridge obtained support this view. In contrast, in the western during our sampling (Woodgate et al., 2001), which Greenland Sea, where Atlantic water of the RAC show that Barents Sea winter water was present on is squeezed in between the GSG and the EGC, the our sampling locations and that the Atlantic Inflow C. finmarchicus population seemed to thrive well on was advected at approximately 5 cm s1 (Woodgate our transect, judging from the presence of spawning et al., 2001). While in the North Atlantic the females despite water temperatures between +11 phytoplankton usually blooms in late spring (Braar- and 1 1C. Apparently its ability to survive long ud et al., 1958), in the Arctic Ocean blooms are periods with little energetic effort makes C. finmar- observed in August/September (Grahl et al., 1999), chicus able to enter far into regions of expatriation. which is several months later. This delay may have Indeed, it is known to over winter for as along caused the gonad absorption observed on Transect as 9 months. CIV, CV, and females can all be F. Indeed, such absorption processes occur when over wintering stages (Hirche, 1996), whereas the females are exposed to long starvation periods younger stages have little to no lipid reserves (Kosobokova, 1999; Niehoff, 2000) and may thus (Kattner and Krause, 1987) and therefore cannot explain their reproductive failure. Feeding super- survive long starvation periods. But which factors abundant food to such females for 11 days induced limit successful development in Polar Regions? egg production only in very few specimens (Hirche Temperature is the factor blamed most often in and Mumm, 1992). Regional differences in the the literature (Jaschnov, 1970; Sameoto, 1984; breeding cycle of C. finmarchicus are common and Tande et al., 1985). It may affect hatching, juvenile were often attributed to differences in the timing of development, gonad maturation, and overwintering phytoplankton development (Huntley et al., 1983; physiology. According to Sameoto (1984), the Plourde and Runge, 1993; Ringuette et al., 2000). stages CII, CIII and CIV have a narrower However, in the Arctic, phytoplankton may develop temperature tolerance than CV and adults. So far just too late to be utilized by C. finmarchicus for there is little knowledge about the effect of sustained gonad maturation. low temperature on the development of C. finmarch- Observations of reproductive activity in the RAC icus, and our study cannot contribute to this issue. and MIZ of the Greenland Sea or near-frontal region Reproductive biology has been studied more of the Barents Sea support the hypothesis of intensively. Previous egg production experiments reproductive failure due to mismatch between the (Hirche, 1990; Hirche et al., 1997) and field timing of the female reproductive cycle and food observations from this study in the MIZ of the availability. In the RAC, specimens ascending into Greenland Sea indicate that temperature per se may the polar layer often find favourable food conditions not be limiting reproduction. in the MIZ. Due to its association with the EGPF, Other factors that may be important for advected this region is ice-free or covered only with thin ice all specimens are the match of food availability and year round. Stability induced by melt water allows intrinsic timing of development. In the North early phytoplankton growth (Smith, 1987). Conse- Atlantic, moulting of adults and subsequent fertili- quently, egg production was found at low tempera- zation of the females by the short-lived males takes tures when food was sufficient (Fig. 3). However, in place in late winter (Marshall and Orr, 1955). When Belgica Trough on the EGS, not far away from the food is available, females produce eggs and spawn. MIZ, but with low food concentrations due to heavy Males were not observed in our samples. The ice cover for most of the year (Lara et al., 1994), no production of males is a sensitive phase in the life signs of growth or reproductive activity were cycle of C. finmarchicus (Irigoien et al., 2000). Either detected (Hirche et al., 1994; Hirche and Kwasniews- male development was inhibited by low tempera- ki, 1997). In the near-frontal region of the Barents tures or they died before our sampling period. Sea, hydrographic conditions are similar to the MIZ The dominance of females in stage composition in in the Greenland Sea. The specimens found there the eastern Arctic Ocean clearly indicates en route may have been advected only recently together with development, assuming that the specimens collected phytoplankton produced in the MIZ. ARTICLE IN PRESS 2744 H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747

5.3. Comparison of C. finmarchicus and C. glacialis female C. glacialis. Thus, a replacement of C. glacialis by C. finmarchicus may happen first only in the later Comparison of the congeners C. finmarchicus and part of the year, when surface temperatures are C. glacialis shows that the latter is at present better surpassing this limit. adapted to life in the Arctic, because it can better Further colonization should depend on the estab- utilize the patchy and mostly late phytoplankton lishment of over wintering populations and changes occurrence that is often associated with polynyas in the regional ecosystem. We assume that it will be such as the Northwater polynya in Baffin Bay crucial whether climate change leads to an earlier (Ringuette et al., 2000), Northeast Water polynya start of phytoplankton development. The transition on the EGS (Hirche et al., 1994; Ashjian et al., 1995, period could be very hazardous to upper trophic 1997; Hirche and Kwasniewski, 1997), and Laptev levels due to the differences in size between the two Sea polynya (Kosobokova and Hirche, 2001). species. C. finmarchicus has a maximum female Females of C. glacialis are long-lived (Kosobokova, prosome length of 3.2 mm as compared to 4.6 mm 1999) and are able to spawn if fed after long in C. glacialis. Correspondingly, maximum carbon starvation periods (Hirche, 1989). The use of ice content is 100–225 mgversus600mg(Hirche and algae (Runge and Ingram, 1988) further expands its Kwasniewski, 1997). Little auks (Alle alle)fromBear growth period. Island only sporadically take the abundant copepod C. finmarchicus, but actively select the much less 5.4. Future perspectives abundant and larger C. glacialis (Weslawski et al., 1999; Karnovsky et al., 2003). Even if mostly inactive, the export of a large biomass of C. finmarchicus represents a big loss for Acknowledgements the North Atlantic, whereas for the Arctic, this export represents both prey for local predators and We thank the captains and crew of the various a large source of carbon that will sink in the areas of RV ‘‘Polarstern’’ cruises. We appreciate the help of expatriation. Under continuing warming and many colleagues who assisted the sampling, experi- strengthening of the Atlantic Inflow, different scenar- ments, sample analysis and preparation of the ios are expected in the future. An increase of advection manuscript, among others R.N. Bohrer, U. Holtz, of Atlantic populations may significantly increase the S. Kwasniewski, D. Mengedoht, U. Meyer and T. sedimentation of advected biogenic material. Further Scherzinger. V. Kosobokov and A. Basilico helped warming could favour the survival of the highly with the maps, R. Schwamborn with the statistics. productive Atlantic communities, which finally could The work of KNK was supported by Russian replace the Arctic fauna, which is characterized by low Foundation for Basic research Grants nos. 03-05- biomass and low production (Hirche and Mumm, 64871 and 06-05-65187 and visiting scientist grants 1992; Kosobokova and Hirche, 2000). Especially in of the AWI. This paper was first presented in the the subarctic shelf seas, a shift from C. glacialis to GLOBEC-ESSAS Symposium on effects of climate C. finmarchicus is likely under continued climate variability on sub-arctic marine ecosystems, hosted change, as not only the survival of C. finmarchicus by PICES in Victoria, BC, May 2005. would be favoured by higher temperatures and earlier blooms due to earlier ice melt, but C. glacialis would be inhibited. Kosobokova (1999) concluded from References comparison of gonad stages and the vertical distribution of C. glacialis collected in the White Sea in Anderson, L.G., Jones, E.P., Koltermann, K.P., Schlosser, P., different years that the key factor causing the Swift, J.H., Wallace, D.W.R., 1989. The first oceanographic section across the Nansen Basin in the Arctic Ocean. Deep- termination of the spawning period of C. glacialis in Sea Research 36, 475–482. early summer was the increase of temperature in the Ashjian, C.J., Smith, S.L., Lane, P.V.Z., 1995. The Northeast surface layer. When daily average temperatures near Water Polynya during summer 1992: distribution and aspects the surface reached 5 1C, females left the surface layers of secondary production of copepods. Journal of Geophysical and stopped spawning. This also was observed in the Research 100 (C3), 4371–4388. Ashjian, C.J., Smith, S.L., Bignami, F., Hopkins, T., Lane, Lurefjord by Niehoff and Hirche (2005).Inboththe P.V.Z., 1997. Distribution of zooplankton in the Northeast White Sea and the Lurefjord, 5 1Cseemstobea Water Polynya during summer 1992. Journal of Marine strong threshold above which dormancy is induced in Systems 10, 279–298. ARTICLE IN PRESS H.-J. Hirche, K. Kosobokova / Deep-Sea Research II 54 (2007) 2729–2747 2745

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