MARINE ECOLOGY PROGRESS SERIES Vol. 308: 101–116, 2006 Published February 16 Mar Ecol Prog Ser

Arctic zooplankton do not perform diel vertical migration (DVM) during periods of midnight sun

Katarzyna Blachowiak-Samolyk1,*, Slawek Kwasniewski1, Katherine Richardson2, Katarzyna Dmoch1, Edmond Hansen3, Haakon Hop3, Stig Falk-Petersen3, Lone Thybo Mouritsen2

1Institute of Oceanology, Polish Academy of Sciences, Powstancow Warszawy Street 55, 81-712 Sopot, Poland 2University of Aarhus, Department of Marine Ecology, University of Aarhus, Finlandsgade 14, 8200 Aarhus, Denmark 3Norwegian Polar Institute, 9296 Tromsø, Norway

ABSTRACT: Diel vertical distribution patterns of dominant zooplankton taxa were studied during a period of midnight sun (May 1999) in the Marginal Ice Zone (MIZ) of the Barents Sea along 2 tran- sects across the ice edge. Eight stations were sampled every 6 h over 24 h at 5 depth intervals. Our study confirmed that copepod nauplii (most probably Calanus hyperboreus and C. glacialis) together with Pseudocalanus spp. preferred the surface water layer. The herbivores C. finmarchicus, C. glacialis, and C. hyperboreus concentrated in the upper 50 m depth interval, whereas the omnivores Metridia longa and Microcalanus spp. were generally found in deeper waters. As a result of vertical distribution patterns of the numerically abundant taxa, a bulk of zooplankton was concentrated within the 0–50 m layer. Vertical distribution patterns of all examined taxa/groups varied in time as a result of habitat changes (with respect to water mass distribution and sea depth) as well as random patchiness. Based on our data and on a comprehensive literature survey on Arctic zooplankton diel vertical migration (DVM), we postulate that common zooplankton taxa in the MIZ of the Barents Sea do not perform DVM under the midnight sun. Arctic C. glacialis in May 1999 occupied deeper layers at stations with more ice cover and less melt water. This distribution pattern was probably related to the species’ reproduction. At the same time, Atlantic C. finmarchicus was concentrated further away from the ice edge and chlorophyll a maximum, and presumably had not begun its seasonal reproduc- tion.

KEY WORDS: Zooplankton · Calanus · Diel vertical migration (DVM) · Marginal Ice Zone · Barents Sea

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INTRODUCTION fishes such as Arctic cod Boreogadus saida, capelin Mallotus villosus, and herring Clupea harengus The Marginal Ice Zone (MIZ) of the Barents Sea is (Dragesund & Gjøsæter 1988). Precise knowledge of the transitional area between open ocean and perma- the diel distribution pattern of pelagic animals in a nent ice cover. It is characterised as one of the most dynamic marine environment is of fundamental impor- dynamic and ecologically important regions in the tance for understanding the trophic relationships world’s oceans because it represents a highly produc- between organisms. tive area in the Arctic (Hegseth 1992, Dayton et al. Diel vertical migration (DVM) is a characteristic 1994, Slagstad & Stokke 1994). Zooplankton play a behaviour of many zooplankton taxa (Longhurst vital role in the Barents Sea ecosystem and the produc- 1976a). In the Arctic, studies of this phenomenon were tion of pelagic zooplankton supports, both directly and initiated by Bogorov (1946), who reported a lack of indirectly, large stocks of commercially important DVM of zooplankton during periods of continuous

*Email: [email protected] © Inter-Research 2006 · www.int-res.com 102 Mar Ecol Prog Ser 308: 101–116, 2006

daylight. This conclusion, however, was not indisput- Trench, to the west and north of the Central Bank. In ably accepted and was a starting-point for later studies the northern Barents Sea and over the Great Bank, the on DVM carried out by Digby (1961), McLaren (1963), upper 150 m of the water column is colder and less Hopkins & Gulliksen (1978), Kosobokova (1978), Buch- saline and is defined as Arctic water (Loeng 1991). This anan & Haney (1980), Falk-Petersen (1981), Groendahl cold Arctic water layer is, initially, formed by freshen- & Hernroth (1986), Runge & Ingram (1988, 1991), ing of Atlantic water by ice melt, by net precipitation, Conover & Huntley (1991), Hays (1995), Hattori & Saito and perhaps also by mixing with less saline water (1997), Dale & Kaartvedt (2000), Fortier et al. (2001), advected from the Kara Sea (Rudels et al. 1991, Steele Arashkevich et al. (2002), and Head et al. (2003). et al. 1995). It is subsequently homogenised during Despite extensive research, the question of whether winter by haline convection in the area of origin, in the Arctic zooplankton migrate diurnally during periods of northern Barents Sea. Then, due mainly to the prevail- constant illumination has not been resolved. ing northerly winds during winter and spring, it is In addition to light, environmental factors such as ice transported south to form the northern component of cover and hydrographic conditions are very important the Polar Front (Vinje & Kvambekk 1991). in determining the vertical distributions of zooplank- Description of transects. This study was a part of the ton (Buchanan & Haney 1980). However, in the programme “Spatial and temporal variability of the Barents Sea, the influence of hydrographic parameters ice-ocean system in the MIZ of the Barents Sea” car- on zooplankton distributions in ice-covered waters has ried out by the Norwegian Polar Institute (Hop & Falk- only been addressed in a few studies (Unstad & Tande Petersen 2003). The investigated area was at the inner 1991, Pedersen et al. 1995a,b, Hansen et al. 1996, Falk- part of the Hopen Trench and surrounding banks of Petersen et al. 1999, Søreide et al. 2003). Thus, our the Barents Sea, from 76°03’N to 77°31’N, and from investigation in the Arctic Barents Sea provided a 26°53’E to 33°08’E (Fig. 1). Zooplankton and hydro- unique, but challenging, opportunity for studying the graphic parameters were collected during a cruise relationship between DVM of zooplankton and hydro- with the ice-strengthened research vessel ‘Lance’ graphy during periods of continuous sun. between 9 and 22 May 1999. Two transects (A: eastern The purpose of the present study was to describe at 33°E, and B: western at 27°E near Hopen), each con- short-term vertical distribution patterns of zooplankton sisting of 4 stations, were sampled from north to south across the MIZ of the Barents Sea, and also address the across the MIZ. Transect A started at the southern question of DVM. While previous studies on DVM phe- Great Bank (<200 m deep) and ended up over deeper nomenon focused either on 1 species/genus or total water in the Hopen Trench (~300 m), whereas Transect zooplankton biomass/abundance, or were based on 2 B started north of Hopen (~200 m) and extended south daily hauls (i.e. day and night), our investigation over the shallower areas of the Spitsbergen Bank allowed us to examine diel changes in vertical dis- (<100 m). Geographical coordinates of each sample are tribution of all the numerically dominant zooplankton given in Hop & Falk-Petersen (2003). The distances taxa in the central Barents Sea, (1) under typical and between the stations varied between 5 and 35 nautical variable MIZ hydrological and ice cover conditions, miles because the primary criterion for their location and (2) during constant illumination. was difference in ice cover condition. Thus, Stns A31 and B49 were in compact pack ice (100%), Stns A33 and B50 were in about 60 to 70% ice cover, Stns A34 MATERIALS AND METHODS and B51 were near the ice-edge in about 10% ice cover, and Stns A35 and B52 were located in the ‘open Study area. The Barents Sea is a continental shelf water’ (Fig. 1). The open water station at the end of the sea with an average depth of 230 m. The physical con- eastern Transect A was located south of the Polar ditions of the sea have been previously described Front; therefore, both ‘across-ice-edge’ and ‘across- (Loeng 1991, Rudels et al. 1991, Steele et al. 1995), so Polar-Front’ conditions were sampled there. Transect B only a brief description of the hydrographic features was located entirely in Arctic water north of the Polar prevailing at the time of the survey is provided. Front. Further details with regard to the ice conditions Typically, in the central Barents Sea, warm Atlantic are described in Engelsen et al. (2002). water from the south encounters cold water from the Environmental background sampling. Ice concen- north over the Hopen Trench, forming the Polar Front tration, ice thickness and floe size were record every at around the 250 m isobath. The inflowing warm and 3 h from the ship and documented using a digital cam- saline Atlantic water is advected northwards by the era (Hop & Falk-Petersen 2003). Norwegian Atlantic Current that splits at the Bear Water mass properties (salinity, temperature and Island Channel. The branch that flows into the Barents density) were measured at each station with a Sea-Bird Sea flows partly north along the axis of the Hopen Electronics SBE 911 + CTD (conductivity, temperature, Blachowiak-Samolyk et al.: Arctic zooplankton migration and midnight sun 103

depth profiler) deployed vertically to the bottom approximately every 3 h. The CTD data were assigned to a grid in MATLAB version 5.3 and contoured Land Josef by linear interpolation (Fig. 2). The Frans °N Nordaust 80 water masses were identified accord- Kvitø ya ing to salinity and temperature proper- landet ties (Loeng 1991, Harris et al. 1998). Information on chlorophyl a (chl a) con- Spitsbergen centration in the study area (mg chl a m–2, integrated for the upper 50 m) used in the discussion was collected parallel to zooplankton sampling but Great only once at each station. Details on Bank sample collection and measurements are described in Engelsen et al. (2002) and Søreide et al. (2003). Hopen 76°N Zooplankton sampling and examina- Bank tion. During sampling the ship was drifting together with the ice and the Spitsbergen05.05.1999 Central Trench underlying near-surface water masses. P Bank Bear Island o The longest distance between start and l Hopen a end sampling a single station, 94 km at r Stn A35 (Fig. 2), was caused by return F ront of the ship to the original start sampling location after the ship had drifted away Maximum extension of sea ice in bad weather conditions. Stratified Minimum extension of sea ice vertical hauls were performed using Atlantic water a multiple plankton sampler (Hydro- Arctic water Bios) consisting of 5 closing nets with Transect A, eastern icetransect Transect B, western icetransect 0.25 m2 square opening and 0.180 mm 20°E mesh. Generally 5 layers were sam- 40°E pled: 0–10 , 10–30 , 30–50 , 50–100 m 30°E and 100 m–bottom, except for 2 sta- 0 100 200 km tions, Stn A34 at 02:15 and Stn B51 at 23:20, where only 4 layers were taken: 0–12 , 12–50 , 50–100 m and 100 m– bottom or 0–10 , 10–30 , 30–50 m, 50 m–bottom, respectively. The lower Fig. 1. Sampling stations and ice extent in the investigated area: Transect A limit of the deepest (bottom) layer sam- eastern (Stns A31, A33, A34 and A35) and Transect B western (Stns B49, B50, B51 and B52) during May 1999. Dates given as d/mo/yr pled was set a few m off the sea bed (typically 5 m off the bottom depth indi- cated by the ship’s echo sounder) to avoid damaging of an ocular micrometer, following standard procedures the net. However, because the location of the net in the (e.g. Harris et al. 2000). water column was determined from the wire length, the The examination of short-term distribution patterns accuracy of setting the distance between the net and was conducted for the most abundant and frequent the bottom varied depending on weather and sea cur- species (Oithona similis, Calanus finmarchicus, C. rent conditions. Each station was sampled every 6 h glacialis, Metridia longa) and genera (Pseudocalanus (5 times) during a 24 h period, and a total of 198 zoo- spp, including P. minutus and P. acuspes, and Micro- plankton samples were obtained. The amount of water calanus spp., including M. pusillus and M. pygmaeus), filtered was calculated based on flow meter measure- as well as for copepod nauplii and for total zooplank- ments for individual samples. Zooplankton samples ton. It was also conducted for C. hyperboreus and Tri- were preserved in 4% borax-buffered formaldehyde conia borealis (=Oncaea borealis) (Böttger-Schnack immediately after sampling. Organisms were identified 1999). We did not consider the appendicularian Fritil- and counted under a stereomicroscope equipped with laria borealis and Euphausiacea larvae because they 104 Mar Ecol Prog Ser 308: 101–116, 2006

Transect A Transect B time (h) time (h) 10:16 16:20 22:07 07:09 07:23 19:28 07:30 13:09 19:20 01:11 04:09 10:13 00:21 04:09 10:16 13:11 16:15 22:02 00:58

20 20 40 40 60 60 80 80 100 100 depth (m) 120 120 140 140 160 B49 160 A31 180 0 2 4 6 8 10 12 14 16 0 2 4 6 8 10 12 14 16 18 distance (km) distance (km) time (h) time (h) 22:20 10:28 11:45 11:13 11:13 18:1301:04 07:47 13:25 20 40 40 60 80 80 100 NO DATA 120 120 AtW depth (m) 140 160 160 MAtW 180 A33 200 B50 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 0 2 4 6 8 10 12 14 16 18 distance (km) distance (km) PFW time (h) time (h) 03:52 16:12 00:56 16:14 BSW 19:16 22:21 01:00 07:14 10:35 13:17 19:24 22:42 04:13 07:06 10:39 13:54 19:28 22:11

20 20 ArW 40 40 60 60 80 80 MMW 100 100 120 MW

depth (m) 120 140 140 160 A34 160 B51 nd 180 180 0 2 4 6 8 10 12 14 16 0 5 10 15 20 25 distance (km) distance (km) time (h) time (h) 07:16 14:13 19:30 02:36 10:49 16:16 19:28 01:08 05:24 10:37 16:11 22:00 00:57 04:04

50 20 100 40 150 60 200 80 depth (m) 250 100 B52 300 A35 120 0 10 20 30 40 50 60 70 80 90 0 2 4 6 8 10 12 14 16 distance (km) distance (km)

Fig. 2. Water masses determined from CTD casts along the 2 transects (A and B) in the Marginal Ice Zone (MIZ), May 1999. Iden- tified water masses were: Atlantic water (AtW), Arctic water (ArW), Polar Front water (PFW), mixed Atlantic water (MAtW), melt water (MW), mixed melt water (MMW), and Barents Sea water (BSW). nd: water masses of not determined type. Bottom contour indicated by oblique line pattern. y: ‘day’ hauls, z: ‘night’ hauls Blachowiak-Samolyk et al.: Arctic zooplankton migration and midnight sun 105

were not present at all stations and their distributions abundance (ind. m–3) of selected zooplankton cate- were very patchy, limited to open water stations and gories occurred as the dependent variable, and time surface layers. Examination of the vertical distribution (‘day’ and ‘night’: distinction according to Fig. 3), ice pattern of C. hyperboreus was made because it is the cover (Group 1: Stns A31, A33, B49, B50 with >50% of third of the Calanus species often indicated as key ice cover; Group 2: Stns A34, A35, B51, B52 with <10% species in the Barents Sea (e.g. Eilertsen et al. 1989, of ice cover) and transect (Transect A, Transect B) as Tande 1991). Triconia borealis was selected because it predictors. Samples were pooled in this way in order to is also regarded as an important zooplankton compo- create ‘replicates’ to enable statistical analysis. Multi- nent in the Barents Sea and other Arctic seas (e.g. ple regression tests were also conducted separately on Arashkevich et al. 2002); however, in our study, each transect. Statistical analyses were conducted with although present at all stations, it was not particularly the Statistical Package of Social Science (SPSS 10.0). abundant. This species was also indicated by Groen- A frequency distribution of Dmax was constructed for dahl & Hernroth (1986) as performing DVM in the every dominant zooplankter selected by counting the Arctic. number of observations of maximum abundance in Visualisations of the short-term distribution patterns each depth interval (0–10 , 10–50 , >50 m). Sample size were completed using Surfer software (Version 7, added up to 40 by pooling samples across transects, Surface Mapping System). Isolines were based on stations and sampling times. Chi-square goodness of zooplankton abundance (ind. m–3) in water layers, fit test was used to determine whether maximum using kriging to determine the distance between lines. abundance depths of each zooplankton were evenly Although variations in light intensity were not mea- distributed amongst layers. Next, a crosstabs chi- sured during the spring cruise (May), diel fluctuations square test was used to test for overall similarity in irradiance would have occurred (Fig. 3). On this between the distributions, followed by pairwise cross- basis, we arbitrarily designated 19:30 to 07:30 h Cen- tabs chi-square tests to determine possible grouping of tral European Time (CET) with lowest photosynthically categories based on their frequency distribution of active radiation (PAR) values as ‘night’ for this study. Dmax. A significance level of 1% was chosen for the This was in agreement with distinction of day/night pairwise crosstabs chi-square tests in order to keep that was applied by Hattori & Saito (1997) in their DVM the statistical analyses conservative focusing on the study from similar latitudes in the Canadian Arctic in general pattern. May 1992. The possible relationship between distribution of Statistics. Multiple regression analyses were applied zooplankton and phytoplankton was tested by linear –2 using the depth interval (Dmax) at which the maximum correlation between daily mean abundance (ind. m ) of selected zooplankton and chl a values (mg chl a m–2) at station. Additionally, the possible relationship between ‘day’ and ‘night’ weighted mean depths Photosynthetically Active Radiation (PAR), May 1999 (WMD) of all dominant zooplankters and chl a values 300 (mg chl a m–2) at station was examined by linear corre- 3May 15 May lation. 250 22 May The non-parametric Mann-Whitney U-test was used to test a possible relationship between zooplankton maximum abundance (ind. m–3) at stations and ice con- ) 200

–2 ditions (Group 1, Group 2).

150 RESULTS PAR(Wm 100 Hydrography and sea ice 50 The water masses of the MIZ were categorised into the following types: Atlantic water (AtW), Arctic water 0 0123456789101112131415161718192021222324 (ArW), Polar Front water (PFW), mixed Atlantic water Time (h) (MAtW), melt water (MW), mixed melt water (MMW), and Barents Sea water (BSW) (Fig. 2). During the sam- Fig. 3. Photosynthetically Active Radiation (PAR) measured at pling period, the ice edge was located near the Polar Bjørnøya (74°N, 20°E) for the period 9 to 22 May 1999, with albedo 0.8 (open sea) and no overcast. Grey areas represent Front in the inner part of the Hopen Trench. On Tran- designated ‘night’ sect A, Arctic water dominated the upper 80 to 100 m 106 Mar Ecol Prog Ser 308: 101–116, 2006

within the ice-covered area (Stns A31, A33, A34), chicus, C. glacialis, C. hyperboreus; (3) >50 m: Micro- whereas mixed and modified waters occurred down to calanus spp., Metridia longa, Triconia borealis (Fig. 4). the bottom. The open water station (A35) was mainly As a result of depth preferences of the numerically characterised by AtW down to 170 m, and mixed/mod- predominating taxa, zooplankton were concentrated ified waters below that depth. On Transect B, the 3 ice in upper layers of the water column (0–50 m) (Fig. 5). stations (B49, B50, B51) were characterised by MW at The maximum concentrations of total zooplankton at the surface and ArW in deeper areas. At the open stations fluctuated from 899 ind. m–3 at Stn A35, to water station (B52), ArW was present at the surface, 6815 ind. m–3 at B49. The distributions of individual whereas mixed or modified water masses occupied the depths below 40 m. The ice conditions at each station changed continu- Table 1. Relative abundance (%) of identified zooplankton ously, depending on wind and tides. The tidal effect along 2 transects in the MIZ of the Barents Sea in May 1999. was very pronounced over the banks and the diver- Examined taxa in bold gence of the tidal wave opened or closed the ice pack on a regular basis. The ice was less than 2 m thick and Transect A Transect B was characterised as first-year ice. Taxon % Taxon %

Oithona similis 46.54 Oithona similis 46.13 Copepod nauplii 18.72 Copepod nauplii 12.69 Taxonomic composition Pseudocalanus spp. 10.19 Calanus glacialis 9.02 Microcalanus spp. 9.42 Pseudocalanus spp. 7.34 Forty-one zooplankton taxa were identified along Calanus finmarchicus 3.20 Fritillaria borealis 5.81 Transect A, whereas 36 taxa were found on Transect B. Calanus glacialis 3.15 Calanus finmarchicus 4.53 2.94 spp. 4.00 The most abundant species in the area was Oithona Fritillaria borealis Microcalanus Metridia longa 2.21 Euphausiacea larvae 3.69 similis, comprising about 46% on both transects, fol- Oithona atlantica 0.64 Echinodermata larvae 0.89 lowed by copepod nauplii and copepods of different Oikopleura spp. 0.48 Calanus hyperboreus 0.75 stages of the genera Calanus, Pseudocalanus, Micro- Echinodermata larvae 0.44 Metridia longa 0.49 calanus, and also Metridia. Of the non-copepod taxa, Triconia borealis 0.35 Oikopleura spp. 0.21 Fritillaria borealis and Euphausiacea nauplii were fre- Euphausiacea larvae 0.32 Triconia borealis 0.20 quently found, and were particularly abundant at Stn Calanus hyperboreus 0.24 Oithona atlantica 0.10 Polychaeta n. det. 0.20 Mollusca larvae 0.07 B52. Among adult Euphausiacea, 4 species were iden- Chaetognatha 0.20 Harpacticoida n. det. 0.07 tified: Thysanoessa inermis, T. raschii, T. longicaudata Hydromedusae 0.15 Chaetognatha 0.06 and Meganyctiphanes norvegica, but they were Amphipoda 0.12 Hydromedusae 0.06 treated together because of their low abundances. Clione limacina 0.10 Clione limacina 0.05 Echinodermata larvae and Chaetognatha were of less Limacina helicina 0.09 Amphipoda 0.04 importance numerically, while remaining taxa were Harpacticoida n. det. 0.05 Polychaeta n. det. 0.03 Euphausiacea adults 0.04 Limacina helicina 0.03 scarcely present (Table 1). Bradyidius. similis 0.04 Euphausiacea adults 0.02 Ctenophora 0.03 Ctenophora 0.01 Ostracoda 0.03 Bradyidius similis 0.01 Short-term distribution of zooplankton taxa Pareuchaeta norvegica 0.02 Scolecithricella minor 0.01 Mollusca larvae 0.02 Isopoda 0.01 The statistical model tested whether the 3 predictors Harpacticoida nauplii 0.02 Ostracoda 0.01 Isopoda 0.01 Harpacticoida nauplii <0.01 (time, ice cover, transect) influenced the . The Dmax Cumacea <0.01 Siphonophora <0.01 overall multiple regression was significant only for Oncaea sp. <0.01 Pareuchaeta norvegica <0.01 Calanus glacialis (Table 2). Partial regression was Scolecithricella minor <0.01 Cumacea <0.01 significant for C. glacialis and ice cover and transect Siphonophora <0.01 Pisces larvae <0.01 (ice cover: partial r = 0.37 p < 0.05; transect: partial r = Cirripedia <0.01 Cirripedia <0.01 –0.37, p < 0.05). Decapoda larvae <0.01 Oncaea sp. <0.01 Pisces larvae <0.01 Decapoda larvae <0.01 The frequency distributions for Dmax of all examined χ2 species/groups were non-random ( 2 > 8.45, p < 0.05) Taxa present on Transect A only 2 and differed between species/groups (χ 16 = 326.8, p < Microsetella norvegica 0.02 0.01). Based on the result of the pairwise crosstabs chi- Neoscolecithrix farrani<0.01 square tests (Table 3), the dominant species/groups were Metridia lucens <0.01 divided into 3 distributional groups according to their Heterorhabdus <0.01 norvegicus D interval: (1) 0–10 m: Pseudocalanus spp., copepod max Gaidius sp. <0.01 nauplii; (2) 10–50 m: Oithona similis, Calanus finmar- Blachowiak-Samolyk et al.: Arctic zooplankton migration and midnight sun 107

Table 2. Results of overall multiple regression between Dmax Number of observations of main zooplankton and selected predictors 0102030 40 0-10 2 Taxon r F3, 28 p

Pseudocalanus spp. 0.069 0.7 0.56 Copepod nauplii 0.10 1.03 0.39 Oithona similis 0.022 0.21 0.89 Calanus finmarchicus 0.18 2.0 0.14 10-50 Calanus glacialis 0.25 3.16 0.04 Calanus hyperboreus 0.092 0.95 0.43

Microcalanus spp. 0.106 1.11 0.36 Depth interval (m) Metridia longa 0.097 1.0 0.41 Triconia borealis 0.12 1.26 0.31 >50 groups are illustrated in Fig. 5 and Appendix 1 (avail- able at: www.int-res.com/articles/suppl/m308p101–116_ Pseudocalanus spp. Calaus hyperboreus app.pdf). copepod nauplii Microcalanus spp. Oithona similis Metridia longa Calanus finmarchicus Triconia borealis Taxa with maximum abundances in Calanus glacialis surface water layer (0–10 m)

Fig. 4. Maximum abundance depth (Dmax) of main zooplankton Pseudocalanus spp. (consisting of P. acuspes and P. minutus) showed highest abundances in the upper water layer (0–10 m) except at 2 stations (A31, B52), Taxa with higher abundances above 50 m where the greatest numbers were found at depths of 10–30 m (Appendix 1a). The highest abundance of The highest concentrations of Oithona similis were these copepods (938 ind. m–3) was found at Stn A34. mainly found at 10–30 and 30–50 m (Appendix 1c). Copepod nauplii demonstrated a similar, but more Oithona similis was most abundant at the ice cover sta- pronounced, pattern of distribution with depth to tions (maximum density 1932 ind. m–3 at Stn B50), and Pseudocalanus spp. The only exception was Stn A31, decreased in abundance at the open water stations where the maximum density occurred within the (A35, B52). 10–30 m depth interval (Appendix 1b). The maximum Maximum concentrations of Calanus finmarchicus abundance (3240 ind. m–3) was observed at Stn A34. occurred within 2 depth ranges: 0–10 and 30–50 m.

2 Table 3. Results of pairwise crosstabs chi-square tests (χ 2 and p) for possible grouping of species based on frequency distribution of maximum abundance depth (May 1999). Significant values shown in bold

Calanus Calanus Calanus Pseudocalanus Microcalanus Metridia Oithona Triconia hyberboreus glacialis finmarchicus spp. spp. longa similis borealis

Calanus glacialis 12.2 <0.002 Calanus finmarchicus 7.8 0.74 0.02 0.69 Pseudocalanus spp. 31.9 7.44 11.7 <0.0005 0.02 0.003 Microcalanus spp. 37.4 51.4 45.2 66.3 <0.0005 <0.0005 <0.0005 <0.0005 Metridia longa 50.6 65.5 59.1 80.0 4.2 <0.005 <0.0005 <0.0005 <0.0005 0.122 Oithona similis 7.8 9.5 8.8 21.2 61.7 76.1 0.02 0.009 0.012 <0.0005 <0.0005 <0.0005 Triconia borealis 20.48 34.0 28.0 50.7 4.1 12.7 41.8 <0.0005 <0.0005 <0.0005 <0.0005 0.13 0.002 <0.0005 Copepod nauplii 48.4 17.3 22.8 6.3 64.7 76.0 40.2 55.7 <0.0005 <0.0005 <0.0005 0.042 <0.0005 <0.0005 <0.0005 <0.0005 108 Mar Ecol Prog Ser 308: 101–116, 2006

total zooplankton time (h) time (h) 08:30 14:00 20:00 02:00 08:00 01:40 08:00 14:20 20:00 02:30 0 0 20 1400 7000

–3 6000 –3 40 1200 50 60 1000 5000 80 800 4000

depth (m) depth (m) 100 3000 100 600

individuals m 2000 individuals m 120 400 200 150 1000 140 A31 B49 0 0

11:20 17:40 00:10 06:00 11:15 11:30 17:45 23:30 05:30 11:30 0 0 4200 2100 1800 50 3500 –3 50 –3 1500 2800 1200 100 100 2100 depth (m) depth (m) 900 1400

individuals m 600 individuals m 150 150 700 A33 B50 300 0 0

20:00 02:15 08:20 14:15 19:45 23:20 05:10 11:30 17:30 23:20 0 0 6000 5000 50 –3 5000 –3 4000 50 4000 3000

depth (m) 100 depth (m) 3000 100 2000

individuals m 2000 individuals m

150 1000 1000 A34 150 B51 0 0

03:15 09:15 15:10 21:15 03:00 06:00 12:10 18:00 00:00 06:00 0 0 800 4000 50 20 700 3500

100 600 –3 40 3000 –3 500 2500 150 60 400 2000 80 depth (m) 200 300 depth (m) 1500 200 1000

individuals m 100 individuals m 250 100 500 A35 120 B52 300 0 0

Fig. 5. Diurnal (24 h) changes in abundance (ind. m–3) of total zooplankton at stations along Transect A and B. Note changes in scale for abundance. Bottom contour indicated by oblique line pattern. Water layers sampled: 0–10, 10–30, 30–50, 50–100 m, and 100 m–bottom. Triangles indicate exact time of sampling. y: ‘day’ hauls, z: ‘night’ hauls according to division from Fig. 3 Blachowiak-Samolyk et al.: Arctic zooplankton migration and midnight sun 109

The maximum abundance at stations fluctuated from light. Another early attempt to tackle the problem was 11 ind. m–3 at Stn B52, to 1259 ind. m–3 at Stn B49 carried out by Digby (1961). The author emphasised (Appendix 1d). the difficulty of extracting a signal of migration from The vertical distribution pattern of Calanus glacialis the very turbulent environments examined (Svalbard (Appendix 1e) was very similar to that displayed by C. fjords). finmarchicus. The highest abundances at stations Later, Buchanan & Haney (1980) stated that zoo- ranged from 60 ind. m–3 at Stn A33 to approximately plankton did not undergo DVM when exposed to con- 2400 ind. m–3 at Stn B49. tinuous daylight in the Arctic. The animals tended to Calanus hyperboreus was more vertically dispersed remain at a constant mean depth, maintaining the in comparison with the other 2 Calanus species, but this same vertical distribution throughout the day. Gron- observation may have been influenced by the low dahl & Hernroth (1986), working in the Nansen Basin numbers recorded in the study (data not shown). It was north and east of Svalbard, concluded that of the 5 numerous at only 2 stations (B51, B52) on Transect B dominating copepods in the area, only Oncaea borealis (maximum densities 95 and 68 ind. m–3, respectively). (=Triconia borealis) and Metridia longa were migra- tors, although they only supported the statement with data for O. borealis. In the seasonally ice-covered seas Taxa with highest abundances below 50 m of Hudson Bay (Canada), Runge & Ingram (1988) showed that females of Calanus glacialis and Pseudo- Microcalanus spp. showed greatest densities below calanus spp. migrated to the food-rich ice-associated 50 m, except at 1 station (A34), where the maximum layer during the night, and carried out a diel feeding abundance occurred in the 30–50 m depth range pattern similar to those observed in open water areas. (Appendix 1f). The maximum abundance (283 ind. In Resolute Passage (Canadian Arctic), Conover et al. m–3) of this species was observed at Stn A34. (1986) observed that, under continuous sunlight, the Metridia longa displayed a clear preference for the vertical migration and diel change in ingestion rate deepest water layer (100 m–bottom) at all stations. Its were related to the tidal cycle. However, the above- highest abundance (71 ind. m–3) occurred at ice- mentioned observations of DVM and diel feeding covered Stn A31 (Appendix 1g). rhythm were exclusively limited to the sub-ice layer. Triconia borealis was more vertically dispersed than Diel migration studies of Arctic and Antarctic zoo- the other copepods studied. The maxima of T. borealis plankton have been reviewed by Conover & Huntley abundances were noted in the 50–100 m depth range (1991). They concluded that in the polar seas, some (data not shown). The species contributed only little to copepods do migrate near mid-summers day but in total zooplankton numbers observed here (maximum their opinion few, if any, studies of zooplankton distri- abundance 10 ind. m–3 at Stn B52). bution have been designed well enough to indisput- A comparison of instances (8 stations) of maximum ably support this statement. A contrasting conclusion abundance during ‘day’ and ‘night’ hauls yielded equal was reached by Dale & Kaartvedt (2000). These numbers for Microcalanus spp. (4:4), Oithona similis researchers claimed that they observed patterns of diel (4:4), copepod nauplii (4:4), and very similar ones for vertical distribution of Calanus finmarchicus during Metridia longa (3:5), whereas visibly higher numbers midnight sun in the Norwegian and Greenland Seas. were observed for ‘night’ hauls for Calanus finmar- They concluded that the differing results with regard chicus (2:6), C. glacialis (1:7), C. hyperboreus (2:6), to diel distribution patterns could indicate plasticity in Pseudocalanus spp. (2:6), and Triconia borealis (2:6). DVM behaviour related to different environmental conditions, and also that some of the differences could be due to sampling design (i.e. fine vertical and tempo- DISCUSSION ral sampling resolutions are needed to reveal subtle changes of distribution patterns). Also, Fortier et al. The phenomenon of DVM of zooplankton was (2001) stated that despite midnight sun, herbivorous described about 50 yr ago as one of the greatest copepods Calanus hyperboreus, C. glacialis and Pseu- puzzles of pelagic natural history (Hardy & Bainbridge docalanus acuspes displayed a normal DVM under the 1954). Since the beginning, studies of this phenome- ice cover in the Barrow Strait in spring: these copepods non have concentrated mainly in temperate and tropi- ascended into the chlorophyll-rich under-ice layer cal areas, whereas less effort has been devoted to the around maximum relative rate of change in irradiance polar regions. Bogorov (1946), who summarized earlier at dusk, but returned to depth a few hours later. studies in the far north, concluded that dominant zoo- Several studies on DVM in zooplankton have been plankton species did not shift their vertical distribution recently conducted in the Barents Sea. Hansen et al. over a 24 h period during the season of permanent day- (1990) noted that Calanus spp. displayed no consistent 110 Mar Ecol Prog Ser 308: 101–116, 2006

day-night vertical migration patterns during spring- confirmed its preference for upper water layers in the summer seasons. Arashkevich et al. (2002) studied sea- Barents Sea during spring. We were, however, unable sonal and spatial changes in biomass of zooplankton in to confirm the suggestion that this species is associated the central Barents Sea and the MIZ during March, with AtW (Melle et al. 1987), as in our study this spe- May and June. They interpreted the difference in cies showed highest abundances in the area covered day/night distribution of total zooplankton at the by sea ice and in association with ArW and MW. This northern stations in May as manifestation of DVM, observation suggests the ability of this species to take although this observation was based exclusively on 2 advantage of unstable environmental conditions which day and night hauls from the same station. are typical in hydrological front areas (Wiborg 1954) In contrast to previous zooplankton studies in the and ice edge zones (this study). Barents Sea, we rigorously analyzed the vertical distri- Generally, calanoid copepods are regarded as the bution pattern of the dominant taxa over a relatively most important organisms that transfer primary large region and with respect to the sea ice cover, production to higher trophic levels in boreal and sub- hydrographic conditions, and time. In the study area Arctic oceans (e.g. Tande 1991, Kwasniewski et al. the dominating taxa were Oithona similis, copepod 2003), although the role of small copepods in these nauplii, Pseudocalanus spp., Calanus finmarchicus, C. waters seems to be underestimated (Arashkevich et al. glacialis, Microcalanus spp. and Metridia longa. In 2002). Key zooplankton species in the Barents Sea are adjacent areas, similar zooplankton compositions were Calanus finmarchicus, which can be used as a tracer of observed in March and May 1998 and in July 1999 by Atlantic water masses, and the typically Arctic C. Arashkevich et al. (2002). However, in June (1995) in a glacialis (Jaschnov 1970). Maximum concentrations of nearby area of the MIZ, zooplankton was predominat- C. finmarchicus and C. glacialis in the 0–50 m depth ed by C. glacialis and P. minutus (Falk-Petersen et al. range during our survey confirmed earlier findings 1999). from the Barents Sea region (Tande & Bamstedt 1985, Over the entire region in May 1999, the characteristic Hassel 1986). However, Hansen et al. (1996) observed feature of the vertical distribution was concentration of that vertical distributions of the 2 species during spring the bulk of the zooplankton in the uppermost layer 1993 were more extensive than in the present study. 0–10 m (Fig. 5). This observation agrees well with re- Sparse occurrence of C. hyperboreus in the area that sults of a study by Pedersen et al. (1995a). However, we studied agrees with findings of Hassel (1986) and each of the numerically important taxa showed individ- points to the fact that this species, in addition to being ual preferences for maximum abundance depth. an Arctic species, is also a deep water copepod that In the Canadian Arctic, Pseudocalanus spp. are thrives first of all in the Greenland Sea and in the Arc- mainly found in neritic waters (Conover & Huntley tic Ocean. Perhaps the reason why C. hyperboreus can 1991). This agrees with our results: lowest numbers of not maintain higher population density in the shelf these copepods were recorded at the deepest and open seas is that, because of its size, it becomes a very easy water station (Stn A35) influenced by AtW. The prefer- prey for benthic and hyperbenthic organisms during ence of the genus Pseudocalanus to upper water layers its wintering at depths. In the Barents Sea there is a observed in our study was in agreement with Melle et great variety of benthic potential copepod predators al. (1987). The report of DVM in Pseudocalanus at high that continue to forage throughout winter (e.g. deep- latitudes (Conover et al. 1988) was not supported by sea shrimp Pandalus borealis and fish such as polar our results. On the contrary, our findings concurred cod Boreogadus saida, Northeast Arctic cod Gadus with those of McLaren (1969), who demonstrated no morhua, and Greenland halibut Reinhardtius hippo- day/night difference in vertical distribution of Pseudo- glossoide) (Dragesund & Gjøsæter 1988). calanus in a fjord on the Baffin Island. Grice (1962) found Metridia longa to be the most fre- The maximum concentrations of copepod nauplii in quently encountered copepod under the permanent our study coincided with ice edge conditions (Stns A31, sea ice, and the third most abundant over the entire A34 and B51) This was in agreement with results of Arctic Ocean. In accordance with previous data (Ped- Falk-Petersen et al. (1999). With regard to depth distri- ersen et al. 1995a, Hansen et al. 1996), we found this bution, Melle et al. (1987) reported that copepod nau- species attained maximum abundance below 100 m. In plii showed preferences for the upper 50 m in the the Norwegian fjords M. longa is known to inhabit Barents Sea. We observed these developmental stages deep waters during both day and night (Balino & to be concentrated in the uppermost 0–10 m of the Aksnes 1993), which is similar to what we observed in water column. the Barents Sea. In the Labrador Sea, Head et al. (2003) According to McLaren (1963), Oithona similis is a found higher densities of this species at night and widespread and numerically important component of argued this could indicate DVM. A similar conclusion epiplankton, especially in the marginal seas. Our study (i.e. of presence of DVM basing on observation of Blachowiak-Samolyk et al.: Arctic zooplankton migration and midnight sun 111

higher densities during night) was formulated by the and C. finmarchicus occurrence in north-eastern Baffin same authors (Head et al. 2003) with respect to Micro- Bay were commonly situated 3 to 4 m above the chl a calanus spp. According to our data, Microcalanus spp. maximum, whereas the distribution pattern of C. hy- showed clear preferences for deeper water layers perboreus coincided with the chl a peak. However, in (below 50 m) in the MIZ of the Barents Sea, and we did some regions, the relationship between Calanus spp. not perceive any indication of DVM for this species. It and chl a distributions has been found to be negative must be mentioned, though, that because of coarse (Woodd-Walker et al. 2001). Flint et al. (2002) even division of the lower part of water column (50–100 and stated, based on investigations of frontal regions, that in 100 m–bottom), recognition of DVM of these deep such environments high zooplankton biomass areas water dwellers may not have been possible given our were located away from the phytoplankton peaks. data if they migrated only within a narrow depth range In this study, the highest chl a concentration in upper (Fortier et al. 2001). 50 m water layer was observed at the open water stations The non-copepod zooplankton, Fritillaria borealis (Stns A35 and B52) and near the ice edge (Stns B51 and and Euphausiacea larvae, were abundant in May 1999 A33). Chl a decreased with distance into the ice covered only on a local basis, notably at the open water sta- region (Engelsen et al. 2002). A similar observation was tion (B52). This was in accordance with previous obser- made in June 1995 in the MIZ (Falk-Petersen et al. 1999), vations of Arashkevich et al. (2002). Based on data from when the chl a concentrations were the highest in the ice the literature (Wiborg 1954) and on our own observa- edge area. Unfortunately, during our study, sampling of tions, we feel inclined to be of the opinion that these chl a was carried out in a different manner (only once species do not perform DVM and prefer upper layers of at a station) to sampling of zooplankton (5 times at a the water column. Euphausiacea larvae are a seasonal station), and the only available information on chl a were component of the Barents Sea zooplankton. Their high integrated biomass for the upper 50 m layers. This abundance during spring is strictly related to spawning, did not allow complex statistical comparison of possible whereas their horizontal/spatial distributions are very relationship between zooplankton and chl a (phyto- much affected by preferences of adult Euphausiacea plankton) depth distribution. for AtW masses (Dalpadado & Skjoldal 1991). We tried, nonetheless, to test for possible relation- A complete study of an ecological phenomenon such ships on more a general level, by calculating linear as DVM should include a proximate and an ultimate correlation between chl a (mg chl a m–2) and daily aspect (Ringelberg & Van Gool 2003). The proximate mean zooplankton abundance (ind. m–2) at stations. As aspect must answer questions on how animals migrate a result, significant negative correlations were found and what physiological and behavioural mechanisms between chl a and integrated abundances of Oithona are involved in migration. The ultimate aspect must similis (r = –0.927, p = 0.003) and Calanus finmarchicus answer why migrations occur, and what adaptive sig- (r = –0.853, p = 0.015). There were no significant corre- nificance can be attributed to the phenomenon. Such lations for any other species/group tested. These find- an approach is, however, not simply realised, and con- ings corroborate the results of Mann-Whitney U-test fusion of proximate and ultimate aspects easily occurs for maximum zooplankton abundance and ice condi- in practice (Ringelberg & Van Gool 2003). Four proxi- tions (see below), which suggested that these 2 species mate factors are considered the most important in this were less abundant at the ice edge and open water respect: light changes, fish presence, food concentra- stations than further off under the ice. In our opinion, tion, and temperature. Several authors agree that the these results may indicate that in the MIZ of the Bar- most important adaptive significance of DVM is avoid- ents Sea in May 1999, C. finmarchicus and O. similis ance of visual predators (McLaren 1963, Gliwicz 1986, did not utilize the phytoplankton bloom related to MIZ, Lampert 1989, Ohman 1990, Dagg et al. 1998, Ringel- probably because of different timing of their life cycles. berg 1999). They argue that zooplankton, such as Another possible explanation for the negative correla- copepods, are complex organisms which must balance tions might be inverse correlation between zooplank- risk of predation and necessity of feeding. Seeking a ton and phytoplankton precisely because of intensive refuge from predators in deeper dark water layers dur- grazing by herbivorous zooplankters, as suggested ing the day and moving to the upper, food-rich layer at previously by Longhurst (1976b). night are considered the main evolutionary benefits Pearre (2003) emphasized the role of food density on acheived by performing DVM. the vertical distribution of zooplankton. According to High zooplankton abundance often coincides spa- Pearre (1979), when animals were in poor condition tially with high chl a concentration (Hansen et al. 1990), due to low food abundance, they were likely to be and food concentration may stimulate diel migratory found near the surface even in daylight; however, behaviour (Conover 1988, and citations therein). Her- because of the increased risk of predation in upper man (1983) observed that peaks of Calanus glacialis waters, they would make short and unsynchronised 112 Mar Ecol Prog Ser 308: 101–116, 2006

escapes to deeper water if they had fed. Conversely, the probability of perception of copepods by predators when in good condition at times of high food abun- relying on vision to find their prey. Summing up, all the dance, they need to spend little time actively foraging above-mentioned authors argued that size would be and would thus spend more time at the deepest end of an important factor in determining whether the zoo- their migration range (Pearre 2003). To verify whether plankton exhibit DVM. In the present study we looked there was any correlation between the mean popula- for patterns in vertical distribution for the entire popu- tion depth and food, we tested for a possible relation- lations of dominant taxa/group. We were not able to ship between chl a values (mg chl a m–2) and ‘day’ and examine differences in depth distribution pattern for ‘night’ WMD of all dominant zooplankters at station. individual developmental stages/size classes; we were The significant linear correlations were found only for not able to collect all stages because of (1) selectivity of Calanus glacialis (‘day’: r = 0.843, p = 0.017; ‘night’: r = the sampling tool, and (2) specifics of the species’ life 0.845, p = 0.017) and C. finmarchicus (‘day’: r = 0.880, cycles. Possibly, we could have examined the relation- p = 0.010; ‘night’: r = 0.892, p = 0.007). Interestingly, a ship between depth distribution and size for popula- negative correlation was found for Triconia borealis tions of Calanus finmarchicus or C. glacialis; however, only when ‘night’ WMD (r = –0.946, p = 0.001) was con- our samples were predominated by copepodite CIII sidered. These findings suggest that mean populations and CIV (data not shown), which previous research depths of herbivores C. glacialis and C. finmarchicus has suggested to be non-migratory. might increase in direct proportion to food richness In DVM studies, the commonly used determinant of (high chl a values) during both ‘day’ and ‘night’; in location of the studied population or selected represen- contrast, the inverse case may apply to the omnivore T. tative in the water column is WMD (Dale & Kaartvedt borealis during ‘night’. After Pearre (1979, 2000, 2003 2000, Irigoien et al. 2004), sometimes called zooplank- and citations therein), the most obvious migrations— ton centre of mass of the vertical distribution (ZCM) and the only migration easily detectable by conven- (Fortier et al. 2001). In our study, use of this determi- tional methods (stratified sampling)—would occur at nant proved inappropriate because of the coarse divi- intermediate food densities, when the population sion of depth layers, especially in the lower part of the migrated more or less as a unit (termed ‘synchronous water column. Instead, we examined the vertical distri- migrations’). bution pattern using Dmax. According to Riley (1976), perceiving DVM of zoo- Changing light level is, generally, regarded as the plankton can also be obscured by the fact that only part most likely cue stimulating vertical migration of zoo- of a population is migratory. He claimed that, in gen- plankton in the water column (Masson et al. 2001). eral, only adult and older stage copepodids are mi- Under continuous light, the rhythm of migratory activ- gratory, and estimated that approximately only half of a ity has been shown to persist for several days before population undertook migration. Kosobokova (1978) disappearing (Andrewartha & Birch 1967). During the observed a weak tendency for migration by adult Arctic spring and summer with continuous sunlight, females of Calanus glacialis in the central Polar Basin the day/night changes in light levels are reduced to during summer. Hays (1995) noted that CV-VI of changes in radiation due to inclination of the sun. C. hyperboreus exhibited a diel variation in depth Digby (1961), working in the Svalbard area, concluded distribution in near-surface layers at temperate lati- that the extent to which DVM occurred during high tudes, although not in the Arctic. Enright & Honegger Arctic summer depended on the extent of the change (1977) reported strong DVM by CV and adults of C. pa- of light intensity as well as on locality. Groendahl & cificus during spring and summer, whereas Dale & Hernroth (1986) stated that the diurnal variation in Kaartvedt (2000) concluded that only CV and females irradiance during the polar summer is large enough to of C. finmarchicus displayed distinctive migrations. produce a pattern of vertical migration similar to that Dale & Kaartvedt (2000) also suggested that the ver- found in temperate latitudes, although DVM may still tical distribution pattern may be affected by an indi- not occur or only be present in some species. vidual’s size. Furthermore, Pearre (1979) argued that Neither the multiple regression nor the partial the swimming capability of zooplankton is directly pro- regression revealed any possible relationship between portional to size. According to Hays et al. (1994), large Dmax and time of day (light level) for the predominant copepod taxa from the northeast Atlantic showed zooplankton in our study. This allowed us to assume significantly stronger DVM than small taxa (<1 mm that there is no DVM in the MIZ of the Barents Sea wide). Haney (1988) explained that immature animals during spring, discernible within the layers distin- may remain in illuminated waters during the day guished. We assumed that the observed variability in because their small size makes them difficult to see. zooplankton abundance could result from sampling at Also, Hays et al. (1994) suggested that copepod size, a station at different times under changing environ- rather than colour, is the principal factor influencing mental conditions (bottom depth or water masses), as a Blachowiak-Samolyk et al.: Arctic zooplankton migration and midnight sun 113

result of the ship drifting, and from water mass move- (Pearre 2003). Similarly, Ohman (1990) concluded that ment (for example, change in abundance of Metridia the DVM phenomenon is dynamic rather than a fixed, longa parallel to change in bottom depth at Stns A34 invariant behavioural trait within a population of a and B49). Thus, we consider that the observed varia- species, and that many individuals within single popu- bility in zooplankton vertical distribution was related lation may perform either reverse, normal, or no DVM. to habitat changes rather than to diel migration According to these conclusions, it seems rather un- pattern. likely to expect to observe all dominant taxa migrating A possible source of variability in zooplankton abun- synchronously in this study. dance could be natural patchiness. Dagg (1977) postu- Another difficulty in investigating zooplankton DVM lated that, in heterogeneous pelagic environments, there using conventional equipment (net sampling) is deter- is a tendency for zooplankton and their food to be mining the number of individuals that remain in close patchily distributed on any spatial or temporal scale. association with the seabed. Due to net construction, a According to Roe (1972), zooplankton is more or less ran- small portion of the water column (usually about 5 m) domly distributed and there is no reason to suppose that close to the bottom was left unsampled during our day and night catches should be equal. Day and night study. Concentration of some zooplankton close to the hauls differed during our study, for example with respect bottom is a known phenomenon and may concern to maximum abundance of the studied taxa. Frequencies hyperbenthic zooplankton, which were beyond the of maximum abundance during day and night were scope of our study, or typical water column dwellers. In equal for Microcalanus spp., Oithona similis, copepod the latter case, the concentrating taxa would be, for nauplii, and Metridia longa, indicating no relationship example, overwintering herbivorous copepods such as with time of sampling (light regime) and suggesting Calanus finmarchicus (e.g. Kaartvedt 1996). We con- patchiness or distribution related to other environmental sider that this inaccuracy would not influence our sam- parameters. On the other hand, frequencies were pling and would not affect results, because our study remarkably higher during the night for Calanus finmar- took place in spring when all the taxa that could possi- chicus, C. glacialis, C. hyperboreus, Pseudocalanus spp., bly exhibit such a behaviour were higher in the water and Triconia borealis, suggesting a systematic difference column as a result of seasonal ontogenetic migration related to time of sampling. However, a closer examina- towards the surface for reproduction. Recently, some tion of the instances of higher abundance during ‘night’ studies revealed that vertical migration can occur in shows that in 2 out of 6 instances for C. finmarchicus, some taxa on much smaller amplitudes (Falkenhaug et C. glacialis and Pseudocalanus spp., this observation al. 1997). If this would be the case, our sampling design coincided with a significant change in another environ- did not allow us to detect such a behaviour. mental condition (i.e. decreasing sea depth at Stns A34 Our investigation revealed a statistically significant and B51), which supported our previous conclusion that negative relationship between Calanus glacialis maxi- there is no DVM in these taxa and that distribution is mum abundance depth and ice cover as predictor, in influenced by other environmental parameters as well as both the multiple regression as well as in partial species’ response to them, rather than light. Additionally, regression analysis. The results suggest that Dmax of the results of Mann-Whitney U-tests revealed no differ- C. glacialis was located at lesser depths in the water ence in the maximum abundance values between ‘night’ column in areas with less ice cover. The influence of and ‘day’ hauls for any analysed taxa. sea ice cover on zooplankton is complex, species It is also noteworthy that almost all the dominant specific, and differs among regions and seasonals. zooplankton considered here had diel peaks of con- Smith (1988) concluded that in summer in Fram Strait, centration at individual stations at the same time the ice edge had a positive effect on herbivorous during the 24 h period. (cf. Appendix 1 & Fig. 5). This zooplankton abundances because of elevated concen- suggests that patchiness related to heterogeneity in trations of plant biomass. However, Hirche et al. (1991) a pelagic environment, rather than synchronised mi- did not find any enhanced biological activities along gration of various taxa related to time (light level), the ice edge in Fram Strait during the same season, accounted for observed differences in zooplankton although he mentioned considerable regional varia- abundance. The phenomenon of DVM is now known bility related to physical mesoscale processes. Similar to be more complex than first assumed. Recently, complex and inconsistent relationships may occur in Pearre (2003) presented an excellent review of the the Barents Sea where, due to dynamic interactions of influence of hunger/satiation state of animals on their sea, ice and atmospheric systems, zooplankton can be vertical movements. Hunger/satiation migrations seem exposed to unusual conditions. to be controlled by individual’s hunger/satiation state, While Hansen et al. (1996) generally observed much and due to its individual character, these migrations lower zooplankton biomasses in the ice edge area com- generally do not result in overall population movement pared to ice cover and open waters in the Central 114 Mar Ecol Prog Ser 308: 101–116, 2006

Barents Sea in May, they recorded the highest egg dance peak concentrated within the upper 0–50 m production rate for Calanus finmarchicus at the ice layer. Pairwise crosstabs chi-square tests revealed 3 edge station. In Disco Bay (West Greenland), which distributional groups amongst the examined can be regarded as a less unpredictable ecosystem, species/taxa according to depth preferences. Pseudo- Hansen et al. (2003) also found no response by Calanus calanus spp. and copepod nauplii were concentrated spp. (all 3 species) to ice cover conditions. We believe within the uppermost water layer (0–10 m). Oithona that a plausible explanation for the generally shallower similis, Calanus finmarchicus, C. glacialis, C. hyper- distribution of C. glacialis in waters with less ice in the boreus preferred the 10–50 m depth interval, whereas MIZ of the Barents Sea in May can be movement of C. Microcalanus spp., Metridia longa, and Triconia bore- glacialis towards the surface, related to the species’ life alis predominantly inhabited waters below 50 m. Verti- cycle (Kosobokova 1999, Kwasniewski et al. 2003). cal distribution patterns varied over time, but neither In addition, the results of the multiple regression and the multiple regression nor the partial regression re- partial regression analysis for transect as predictor vealed any possible relationship with time of day (light seem to support our hypothesis that the vertical distri- level). We hypothesized that the studied taxa do not bution of Calanus glacialis was predetermined by the perform DVM in the MIZ of the Barents Sea in spring. species’ life cycle. Both analyses yielded significant We assumed that both habitat changes (in respect of negative relationships between the maximum abun- water mass distribution and sea depth) and random dance depth of C. glacialis and transect, thus indicat- patchiness could account for observed variability in ing that Dmax for this species was greater on Transect A zooplankton vertical distribution. The results of multi- than on Transect B. Samples on Transect A were col- ple regression and partial regression indicate that, in lected earlier (9 to 14 of May) than on Transect B (17 to the MIZ in spring, C. glacialis occupied deeper layers at 21 of May), and there was less melt water on Transect stations with more ice cover and less melt water. Such A. We postulate that C. glacialis on Transect A was behaviour is most likely related to the species’ life generally located deeper in the water column than on cycle. Among other examined species/taxa, statistically Transect B, because the species was less advanced in significant relationships were found only among the its seasonal vertical migration towards the surface. distributions of C. finmarchicus and O. similis and ice The non-parametric Mann-Whitney U-test indicated and chl a. In the MIZ in spring, both species were a possible relationship between ice conditions and concentrated further away from the ice edge and chl a maximum abundance of copepod nauplii (p = 0.027), maximum. We presumed that this was related to differ- Oithona similis (p = 0.001), Calanus finmarchicus (p = ences in the timing of their life cycles. We also observed 0.002), and C. hyperboreus (p = 0.018). Copepod nau- significantly higher abundances of copepod nauplii and plii and C. hyperboreus were generally more abundant C. hyperboreus (mostly CI) in relation to ice edge. All at the ice edge and open water stations than at the ice the mentioned above findings allowed us to hypo- cover stations (mean maximum abundance 952 versus thesize that, during our study, the reproducing cope- 510 and 26 versus 2 ind. m–3, respectively). Although pods were C. hyperboreus and C. glacialis, whereas not confirmed by correlation analyses, higher abun- C. finmarchicus had not yet begun reproduction. dances of copepod nauplii and C. hyperboreus (mostly copepodids CI) coincided with generally higher chl a Acknowledgements. We thank T. Svenøe for help with the values at the ice edge and open water stations; this PAR figure. We acknowledge the captain and crew of the RV ‘Lance’ for ship logistics and assistance in the field. We also corroborates with earlier findings that suggested a pos- thank the Norwegian Polar Institute (Tromsø), the Institute of itive relationship between copepod reproduction and Oceanology (Sopot), and the partners of the Barents Sea Pro- the amount of available food (Herman 1983). On the duction Licenses 182, 225 and 228 (Norsk Hydro, Statoil, contrary, O. similis and C. finmarchicus were less abun- Agip, Chevron, Neste, Enterprise, SDØE: contract No. 9000000465) for their financial and technical support. This dant at the ice edge and open water stations (631 versus project was also partly supported by a grant from the Euro- –3 1079 and 43 versus 220 ind. m , respectively). We pre- pean Commission programme ‘Transitional Access to Major sumed that at the time of our study, reproduction of C. Research Infrastructures’, COBICE project (contract no. hyperboreus and C. glacialis was already taking place, HPRI-CT-2001-00129). 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Editorial responsibility: Otto Kinne (Editor-in-Chief), Submitted: July 26, 2004; Accepted: August 18, 2005 Oldendorf/Luhe, Germany Proofs received from author(s): January 17, 2006