Ice in the Environment: Proceedings of the 16th IAHR International Symposium on Ice Dunedin, New Zealand, 2nd–6th December 2002 International Association of Hydraulic Engineering and Research

COPEPODS IN ARCTIC PACK ICE AND THE UNDERLYING WATER COLUMN: LIVING CONDITIONS AND EXCHANGE

PROCESSES

Iris Werner1, Klaus Meiners2 and Henrike Schünemann1

ABSTRACT Copepods (e.g. Tisbe, Halectinosoma, Cyclopina) are a major group of the sympagic meiofauna. Highest abundances are often observed in the bottom part of the ice and in the water layer directly below the ice, indicating most favourable living conditions there. During the expedition ARK XVI/2 (August 2000) with the icebreaker RV “Polarstern” to the Greenland Sea and Fram Strait (Arctic), whole sea-ice cores and under-ice water samples down to 5 m depth were studied for species diversity, abundance and vertical distribution of sympagic copepods. Although the copepods occurred in much higher concentrations in the ice, they were also found in considerable numbers in the under-ice water layer, indicating that either active migration or passive transportation, e.g. by flushing meltwater in summer, between the two systems takes place. In this paper, results of two selected stations will be presented and the possible role of migrating sympagic copepods for cryo-pelagic coupling processes, e.g. transfer of organic matter through feeding activity, will be discussed. INTRODUCTION Sea ice in both hemispheres is not only an important factor influencing climate, hydrography and geology, but also forms a unique habitat for a highly specialized so-called sympagic (= with ice) flora and fauna (e.g. Horner et al., 1992). The brine-channel system within the ice (Weissenberger, 1992) as well as the ice-water boundary layer (Werner, 1997) form distinct sub-systems of this habitat, but are connected by a variety of cryo-pelagic coupling processes (Gradinger, 1998). Copepods, above all members of the sub-orders Harpacticoida and Cyclopoida, are a major group of the sea-ice meiofauna, both in the Arctic (Gradinger, 1999) and in the Antarctic (Schnack-Schiel et al., 2001). About 15 species have been described for the Arctic so far. The majority of studies on sympagic copepods in and below Arctic sea ice have been conducted in coastal fast ice over shallow waters in the Canadian and Alaskan Arctic (Carey and Montagna, 1982; Grainger and Mohammed, 1986). The only description of sympagic copepod species in the under-ice

1 Institute for Polar Ecology, Wischhofstr. 1–3, Geb. 12, D-24148 Kiel, Germany, iwerner@ipoe.uni-

kiel.de 2 Yale University, Department of Geology and Geophysics, Box 208109, New Haven, CT 06520-8109

USA

water layer in the Eurasian Arctic comes from the Laptev Sea and the adjacent Arctic Ocean (Werner and Martinez, 1999). Integrated abundance and biomass data of sympagic copepods from pack ice in the Central Arctic Ocean have been published by Gradinger (1999), but without information on the occurrence of the copepods in the under-ice water layer. In this paper, we will present data on species diversity, vertical distribution and abundance of sympagic copepods in pack ice and the under-ice water in Fram Strait, the connection between the Arctic and the North Atlantic Ocean. Furthermore, we will discuss the possible role of migrating sympagic copepods for cryo-pelagic coupling processes, e.g. by transfer of organic matter through feeding activity. MATERIAL AND METHODS The material for this study was sampled during the expedition ARK XVI/2 with RV “Polarstern” to the Fram Strait in August 2000 (Krause and Schauer, 2001). The Fram Strait is the only deep-water connection between the Arctic Ocean and the North Atlantic (Coachman and Aagaard, 1974) and a major export area for sea ice (Wadhams, 1983). Ice conditions in the study area (Fig. 1) were very heterogenous during the cruise with the pack-ice cover varying from 1/10 to 10/10, floe sizes of <1 m to >100 m, and a mixture of many different ice classes (young ice, first-year ice, multi-year ice) of respectively different ice thicknesses (10–350 cm). All ice stations were most probably on multi-year ice, since ice thickness on the stations was always well above 2 m. With the exception of station 224, ice stations were over deep water (>1000 m). In this paper, only results from two selected stations (221, 228) are shown. Station numbers are days of the year.

Figure 1: Study area and position of ice stations during the expedition ARK XVI/2 (August 2000) to the northern Greenland Sea and Fram Strait (Arctic). Station numbers = days of the year.

On each ice station, two ice cores (named A and B) were obtained with a motor-powered CRREL type ice corer (internal diameter: 9 cm). Ice core A was used for the determination of ice temperature, bulk salinity, algal pigments (chl a) and particulate organic carbon (POC). Ice temperatures were measured with a Testo720-thermometer immediately after collection inside small holes drilled into the core in 2–10 cm intervals. Thereafter the ice core was cut into 1–20 cm sections, which were placed in clean polyethylene boxes. Ice segments were transported to the ship and melted in the dark at 4 °C. Salinity of the melted segments was measured with a WTW 190 conductometer. Subsamples (30–400 ml) were filtered onto Whatman GF/F filters and analysed fluorometrically for chl a with a Turner Designs 10-AU digital fluorometer according to Arar and Collins (1992). The remainder of the melted segments (70–1000 ml) was filtered onto pre-combusted Whatman GF/F filters and used for the determination of POC with a CARLO ERBA NA 1500 CHN-Analyzer (Verardo et al., 1990). Based on the temperature and salinity measurements, brine salinity was calculated as a function of ice temperature (Assur, 1958) and brine volume as a function of ice temperature and ice bulk salinity (Frankenstein and Garner, 1967, Leppäranta and Manninen, 1988). Ice core B was used for the determination of metazoan abundance. The ice core was cut into 1–20 cm sections which were melted by addition of 0.2 µm prefiltered seawater at 4 °C in the dark (Garrison and Buck, 1986). Melted ice samples were poured through a 20 µm mesh and the concentrated metazoans were fixed with borax-buffered formalin (4 % final concentration). Metazoans were identified and counted under a WILD MZ8 dissecting microscope (Friedrich, 1997). Temperature and salinity profiles (resolution of 10–100 cm) in the under-ice water (0–5 m depth below the ice underside) were determined in situ with a WTW 190 thermo- and conductometer lowered through a core hole. Water samples for the determination of algal biomass (chl a) and particulate organic carbon (POC) were collected through core holes using a polyethylene tube (internal diameter: 4.0 cm) with a valve at one end. The other end of the tube (equipped with a 8 kg weight) was lowered into the water with the valve open. At the sampling depth (0, 1, 2, 3, 4, 5 m below the ice underside) the valve was closed and the tube with the trapped water was retrieved. Analysis of the water samples was according to the melted ice cores. Quantitative samples of the sub-ice fauna were collected from the same depth strata like the water samples by an under-ice pumping system equipped with a standardized water meter and a tube lowered through a core hole. Organisms gained through this pump were concentrated on a 50 µm mesh gauze inside the sampling pot (Werner and Martinez, 1999) and identified and counted under a WILD MZ8 dissecting microscope. In this paper, only results on the sympagic copepods in and below the ice are shown. RESULTS Temperature and salinity Sampling period was in the first half of August (stn 221: 8.8.2000, stn 228: 15.8.2000). Temperatures in the ice showed strong vertical gradients with summerly high (stn 221) or just decreasing (stn 228) values at the ice surface and lowest values close to the freezing point at the ice underside (Fig. 2). According to the ice temperature, the calculated brine salinity showed strong gradients, too, with low values at the ice surface and highest values similar to the seawater at the ice underside (Fig. 2). In the under-ice water, no gradients of temperature or salinty were found at either station, however, the two stations differed

considerably regarding under-ice hydrography: At stn 221, there was a difference of about 1 °C between the lowermost ice segment and the uppermost water layer analyzed, temperature in the under-ice water was higher than in the ice and well above the freezing point (Fig. 2A). In contrast, at stn 228 temperatures at the ice underside and in the under-ice water were nearly the same and close to or at the freezing point (Fig. 2B).

0

50

100

150

200

0 5 10 15 20 25 30 35 40Salinity

Dep

th in

ice

[cm

]

ICE

TS

0

100

200

300

400

500

6000-0.5-1.0-1.5-2.0-2.5

Temperature [°C]

Dep

th b

elo

w ic

e [c

m]

WATER

TTF S

A0

50

100

150

200

250

0 5 10 15 20 25 30 35 40Salinity

0

100

200

300

400

500

600-2.5 -2.0 -1.5 -1.0 -0.5 0

Temperature [°C]

T

T

TF S

S

TemperatureFreezing temperature(Brine-) Salinity

B

Figure 2: Temperature and salinity profiles in ice and underlying water column at A) Stn 221, and B) Stn 228. Salinity in the ice is calculated brine salinity. T = temperature, TF = freezing temperature, S = (brine) salinity. Algal pigments and organic matter Calculated brine volume in the ice generally increased from the surface to the underside of the ice at both stations (Fig. 3A,B). At stn 221, algal pigments as a measure of biomass followed brine volume and showed highest values in the lowermost decimetres of the ice. Compared with this bottom part of the ice, there was less algal biomass in the under-ice water (Fig. 3A). At stn 228, the distribution of algal biomass was not consistent with brine volume. Here highest values for algal biomass were found in the upper decimetres of the ice, and compared to the bottom part of the ice, there was an equal concentration of algal

biomass in the under-ice water (Fig. 3B). Algal biomass in the ice and in the under-ice water was higher by one order of magnitude at stn 221 than at stn 228. Particulate organic carbon (POC) showed highest concentrations in the upper part of the ice at both stations, and compared to the bottom part of the ice, more POC was found in the under-ice water (Fig. 3C,D). Concentrations of POC were comparatively similar at both stations.

0 0.2 0.4 0.6 0.8 1.0 1.2 1.4

0-2020-4040-6060-80

80-100100-120120-140140-160160-180

180-203.5203.5-209.5209.5-211.5211.5-212.5

212-213.5Water 0-500

Algal biomass [µg Chl a l-1]

Brine volume [%]

Dep

th in

ice

[cm

]

6 8 10 12 14

0 2

2 4 6 8 10 12

30

4 6 8 10

0-2020-4040-6060-80

80-100100-120120-140140-160160-180180-200200-220220-240

240-249.5249.5-255.5255.5-257.5257.5-258.5258.5-259.5Water 0-500

Algal biomass [µg Chl a l-1]

Brine volume [%]

0 100 200 300 400 500

Organic Carbon [µg POC l-1]

no data

0-2020-4040-6060-80

80-100100-120120-140140-160160-180

180-203.5203.5-209.5209.5-211.5211.5-212.5

212-213.5Water 0-500

Dep

th in

ice

[cm

]

0 200 400 600 800 1000 1200

20-40 0-20

40-6060-80

80-100100-120120-140140-160160-180180-200200-220220-240

240-249.5249.5-255.5255.5-257.5257.5-258.5258.5-259.5Water 0-500

Organic Carbon [µg POC l-1]

Stn 221

Stn 221 Stn 228

Stn 228A B

DC

Figure 3: Vertical profiles of brine volume and algal biomass (upper graphs) and particulate organic carbon (lower graphs) in ice and underlying water column at stn 221 (A, C) and stn 228 (B, D). Note different scales.

Copepods Several species of copepods were observed in the ice and/or in the under-ice water (Table 1). Only the results of the truly sympagic copepods Halectinosoma spp. (with probably two species: H. finmarchicum and H. neglectum), Tisbe spp. (with T. furcata and probably some undescribed species) and Cyclopina spp. (with Cyclopina schneideri and probably one or two more species) will be shown here in detail. Oithona similis and Oncaea borealis both occur regularly in the under-ice water, O. similis is a very abundant and dominant species in this habitat. However, these two species were only found in very low numbers at one station inside the ice. The truly pelagic species Microsetella norvegica, Calanus spp.

(C. finmarchicus, C. glacialis, C. hyperboreus), Pseudocalanus spp. (P. minutus, P. acuspes) and Jaschnovia brevis were never found in the ice, but always in the under-ice water. Table 1: Species of copepods from pack ice and under-ice water found during the expedition ARK XVI/2 to the Fram Strait (Arctic)

Species Usual habitat Found in ice Found in under-ice water Halectinosoma spp. Ice +++ +++ Tisbe spp. Ice/Water +++ +++ Cyclopina spp. Ice + +++ Oithona similis Water + +++ Oncaea borealis Water + +++ Microsetella norvegica Water - +++ Calanus spp. Water - +++ Pseudocalanus spp. Water - +++ Jaschnovia brevis Water - +++ + = at a single station, ++ = at more than a single station, +++ = at each station Highest abundances of sympagic copepods were found in the lowermost 10 cm at both stations, with a clear dominance of Halectinosoma spp. (Fig. 4A,B). Only single specimens occurred in higher ice segments. At stn 221, this distribution corresponds to the vertical profile of brine salinity (Fig. 2A), brine volume and algal pigments (Fig. 3A), but not to the distribution of POC (Fig. 3C) in the ice. At stn 228, it corresponds only to brine salinity (Fig. 2B) and brine volume (Fig. 3B), but not to algal pigments (3B) or to POC (Fig. 3D) in the ice. Concentrations of copepods in the lowermost parts of the ice were higher by two to three orders of magnitude as compared to concentrations in the under-ice water. Sympagic copepods occurred down to 5 m water depth at both stations, again with a strong dominance of Halectinosoma spp., although Tisbe spp. had a higher relative share here than in the ice (Fig. 4C,D). At stn 221, copepod abundance were highest directly at the ice-water interface and decreased with water depth (Fig. 4C). In contrast, at stn 228, copepod abundances did not show any distinct distribution pattern (Fig. 4D). Concentrations of copepods were about three times higher in the under-ice water at stn 221 as compared to stn 228 (Fig. 4C,D). Egg-carrying females and different developmental stages of all copepod species were observed. Discussion The genera and species of sympagic copepods found in the ice and in the underlying water layer during the present study in Fram Strait (Halectinosoma spp., Tisbe spp., Cyclopina spp.) have also been observed in other areas of the Arctic, in particular in and below nearshore fast ice in shallow waters in the Canadian and Alaskan Arctic (Carey and Montagna, 1982; Grainger and Mohammed, 1986; Grainger and Hsiao, 1990). These species are of benthic origin, inhabiting shallow habitats like the intertidal or coastal phytal on the Arctic shelves (Lang, 1948; Montagna and Carey, 1978) from where they are believed to colonize the sea ice like an “upside-down-benthos” (Carey and Montagna, 1982; Grainger, 1991; Carey, 1992). The pack ice sampled in Fram Strait has been above deep water, probably for a long time, assuming that this ice came from the Central Arctic Ocean with the Transpolar Drift (Wadhams, 1983). Populations of sympagic copepods over deep water, far away from the source areas, can only be sustained when reproduction takes place in the ice. This is supported by the observation of egg-carrying females and all

developmental stages of copepods in the ice (Grainger et al., 1985; Friedrich, 1997; own observation). The large-scale circulation patterns of pack ice provide a transport mechanisms for a remarkably similar ice and under-ice fauna throughout the Arctic Ocean and its marginal seas (Grainger and Hsiao, 1990).

0 100 200 300 400

0–2020–4040–6060–80

80–100100–120120–140140–160160–180180–200200–206206–212212–214214–215215–216

Abundance [ind. l-1]

ICE

Dep

th in

ice

[cm

]

0 100 200 300 400

0

100

200

300

400

500

Abundance [ind. m-3 ]

Dep

th b

elow

ice

[cm

]

WATER

0 20 40 60 80 100

0–2020–4040–6060–80

80–100100–120120–140140–160160–180180–200200–220220–240240–260260–267267–273273–275275–276276–277

Abundance [ind. l-1]

ICE

HalectinosomaTisbeCyclopina

0 20 40 60 80 100

0

100

200

300

400

500

Abundance [ind. m-3]

WATER

Stn 221 Stn 228A B

DC

Figure 4: Vertical distribution of dominant species of sympagic copepods in ice (upper graphs) and underlying water (lower graphs) at stn 221 (A, C) and stn 228 (B, D). Note different scales. The copepod assemblage in ice and under-ice water layer was characterized by low species diversity and high abundance of one dominant species (Halectinosoma finmarchicum), a typical feature for sympagic copepods both in the Arctic and in the Antarctic, where much more species of copepods inhabitat the pelagic and benthic habitats (Carey, 1992; Werner and Martinez, 1999; Swadling et al., 2000). This low diversity probably reflects that only a few species have developed the necessary adaptations for a successful colonization of the sea-ice ecosystems (Swadling et al., 2000). However, some as yet undescribed species in Arctic sea ice may underestimate the species diversity here. Abundances of sympagic copepods were always higher in the ice than in the underlying

water layer by 2–3 orders of magnitude, indicating that the ice interior is their primary habitat. This is in general accordance with studies from near-shore ice, although there the colonization patterns vary with the seasonal freezing-melting-cycle of the ice (Grainger et al., 1985; Grainger and Mohammed, 1986). Multi-year pack ice over deep water is the habitat for the sympagic copepods year-round, thus it would be expected that the copepods stay close to the ice. This is demonstrated in the vertical profile of stn 221 with highest abundances of copepods in the upper metre of the water layer, probably the typical case. The brine-channel system within sea ice on the one hand and the underlying water column on the other hand are two totally distinct habitats with different environmental conditions. Organisms living in either habitat have to be adapted to the respective conditions. Moreover, organisms like sympagic copepods which occur in both habitats must have developed adaptations for the changing conditions when changing the habitat. This is especially evident for the temperature and salinity regime in the two habitats. Sympagic copepods clearly prefer the lower part of the ice where these factors are comparatively moderate (Gradinger et al., 1999; present study). A meltwater layer below Arctic sea ice is a common feature during summer (Grainger and Mohammed, 1986; Eicken, 1994; Gradinger, 1996), therefore organisms in this water layer must have special adaptations to endure the osmotic stress resulting from extreme and fluctuating temperature and salinity conditions. Sympagic copepods have shown salinity tolerances in the range of S = 20–70, both in the Arctic (Grainger and Mohammed, 1990) and in the Antarctic (Dahms et al., 1990), indicating the ability to cope both with low salinities during melting in summer and with high salinities during freezing in winter. An unsolved question is whether the organisms migrate actively between pack ice and water column or whether they are passively transported by physical processes like meltwater flushing (Grainger and Mohammed, 1986; Fortier et al., 1995). With meltwater present, more sympagic copepods are found below the ice then without meltwater (Werner and Martinez, 1999; this study). Gravity drainage and brine expulsion during freezing are potential transport mechanisms from the ice to the water in winter (Maykut, 1985), distribution and abundance data from the winter are needed for an insight into the latter point. In contrast to the free water column, the brine channels inside the ice represent a defined space with solid surfaces. The inhabitable pore space of channels and pockets in the ice is a direct function of temperature and bulk salinity (Frankenstein and Garner, 1967) and a limiting factor for the size distribution of organisms (Krembs et al., 2000). As an overall mean diametre of channels, a value of 200 µm has been given (Weissenberger, 1992). The mean width of Arctic sympagic copepods, whose body shapes are generally elongate, varies between 160 µm for Halectinosoma sp. and 250 µm for Tisbe spp. (Friedrich, 1997). Corresponding to the temperature and salinity profiles in the ice during summer, the highest brine volume and probably also the widest brine channels occur in the lowermost part of the ice, together with the highest abundances of copepods. Moving along solid surfaces or swimming in a free water column are two different modes of moving. The sympagic copepods Drescheriella glacialis (Tisbidae) and Harpacticus furcifer from Antarctic sea ice have shown good swimming abilities (Dahms et al., 1990), as have the Arctic species Tisbe spp. and Cyclopina spp. (Hauspie and Polk, 1973; own observations). The question rather is, how these copepods move inside the brine channels, here new methods for experimental or in situ studies like endoscopic observations are needed. Although sympagic copepods are believed to feed mainly on ice algae (Grainger and

Hsiao, 1990, Grainger, 1991), their distribution did not always correspond to the distrib-ution of algal biomass and particulate organic matter in the ice during the present study. It is likely that the abiotic factors temperature, salinity and brine volume set the limits towards the upper part of the ice for the copepods, but there is not such a strong limit towards the under-ice water layer. The sympagic copepods have mouthpart structures adapted to holding and grasping prey from surfaces rather than for suspension feeding (Grainger and Hsiao, 1990, Grainger, 1991). It is therefore more likely that the copepods mainly feed inside or from the underside of the ice and not in the free water column. Nothing is known about the fate of faecal pellets produced and released by sympagic copepods, which may be released to the water column. Faecal pellets produced by pelagic copepods are regarded as an important vehicle for a fast and effective vertical transport of organic matter (Tremblay et al., 1989; Lampitt et al., 1990). Under-ice amphipods feed at the ice underside and release faecal pellets into the water column, providing a direct flux of organic matter between the sea ice and the pelagic realm (Werner, 2000). However, harpacticoid sympagic copepods have been found in the guts of Arctic under-ice zooplankton like the ctenophore Mertensia ovum or the amphipod Themisto libellula as well as in fish like polar cod Boreogadus saida from the under-ice habitat (Bradstreet and Cross, 1982; Carey and Boudrias, 1987; Grainger and Hsiao, 1990). Furthermore, exper-iments have shown that the under-ice amphipod Gammarus wilkitzkii effectively preys on sympagic copepods like Halectinosoma finmarchicum (Werner et al., 2002). Thus, sympagic copepods migrating between ice and water transfer ice-produced organic matter on which they feed inside the ice to predators in the underlying water column. When the pack ice finally melts on its way south in the Greenland Sea (Martin and Wadhams, 1996), sympagic copepods will definitely lose their habitat and will be released into the water column. A combination of mean biomass and ice flux data estimated an input of 4 ×103 t C y–1 by sympagic copepods in the major melting area of the Greenland Sea (Gradinger et al., 1999). The further fate of these members of the sea-ice meiofauna is unknown and requires future research. ACKNOWLEDGEMENT We like to thank captain and crew as well as the chief scientist U. Schauer during ARK XVI/2 for constant support and co-operation. The help of many colleagues and polar bear watchers out on the ice is gratefully acknowledged. Annette Scheltz conducted some analysis of chlorophyll and POC. This work was partly funded by the Deutsche Forschungsgemeinschaft (WE 2536/1 and SP 377/9-1-3). REFERENCES Arar, E.J. and Collins, G.B. Method 445.0: In Vitro Determination of Chlorophyll A and

Pheophytin A in Marine and Freshwater Algae by Fluorescence. U.S. Environmental Protection Agency Publ 445: 1–17 (1997).

Assur, A. Composition of Sea Ice and its Tensile Strength. National Research Council Publication 598: 106–138 (1958).

Bradstreet, M.S.W. and Cross, W.E. Trophic relationships at high Arctic ice edges. Arctic 35: 1–12 (1982).

Carey, A.G. The ice fauna in the shallow southwestern Beaufort Sea, Arctic Ocean. Journal of Marine Systems 3: 225–236 (1992).

Carey, A.G. and Boudrias, M.A. Feeding ecology of Pseudolibrotus (= Onisimus) litoralis

Kröyer (Crustacea: Amphipoda) on the Beaufort Sea inner continental shelf. Polar Biology 8: 29–33 (1987).

Carey, A.G. Jr. and Montagna, P.A. Arctic sea ice faunal assemblage: first approach to description and source of underice meiofauna. Marine Ecology Progress Series 8: 1–8 (1982).

Coachman, L.K. and Aagaard, K. Physical oceanography of Arctic and Subarctic Seas. Springer, New York (1974) 72p.

Dahms, H.-U., Bergmans, M. and Schminke, H.K. Distribution and adaptations of sea ice inhabiting Harpacticoida (Crustacea, Copepoda) of the Weddell Sea (Antarctica). Marine Ecology 11: 207–226 (1990).

Eicken, H. Structure of under-ice melt ponds in the central Arctic and their effect on the sea-ice cover. Limnology and Oceanography 39: 682–694 (1994).

Fortier, L., Fortier, M. and Demers, S. Zooplankton and larval fish community development: comparative study under first-year sea ice at low and high latitudes in the northern hemisphere. In Proceedings NIPR Symposium Polar Biol. 8: 11–19 (1995).

Frankenstein, G. and Garner, R. Equations for determining the brine volume of sea ice from –0.5° to –22.9 °C. Journal of Glaciology 6: 943–944 (1967).

Friedrich, C. Ecological investigations on the fauna of the Arctic sea-ice. Berichte zur Polarforschung 246: 1–211 (1997).

Garrison, D.L. and Buck, K.R. Organism losses during ice melting: a serious bias in sea ice community studies. Polar Biology 6: 237–239 (1986).

Gradinger, R. Integrated abundance and biomass of sympagic meiofauna in Arctic and Antarctic pack ice. Polar Biology 22: 169–177 (1999).

Gradinger, R. Life at the underside of Arctic sea ice: biological interactions between the ice cover and the pelagic realm. Memorandum Society Fauna Flora Fennica 74: 53–60 (1998).

Gradinger, R. Occurrence of an algal bloom under Arctic pack ice. Marine Ecology Progress Series 131: 301–305 (1996).

Gradinger, R., Friedrich, C. and Spindler, M. Abundance, biomass and composition of the sea ice biota of the Greenland Sea pack ice. Deep-Sea Research II 46: 1457–1472 (1999).

Grainger, E.H. Exploitation of Arctic sea ice by epibenthic copepods. Marine Ecology Progress Series 77: 119–124 (1991).

Grainger, E.H. and Hsiao, S.I.C. Trophic relationships of the sea ice meiofauna in Frobisher Bay, Arctic Canada. Polar Biology 10: 283–292 (1990).

Grainger, E.H., Mohammed, A.A. and Lovrity, J.E. The sea ice fauna of Frobisher Bay, Arctic Canada. Arctic 38: 23–30 (1985).

Grainger, W.H. and Mohammed, A.A. Copepods in Arctic sea ice. Syllogeus 58: 303–310 (1986).

Hauspie, R. and Polk, P. Swimming behaviour patterns in certain benthic harpacticoids (Copepoda). Crustaceana 25(1): 95–103 (1979).

Horner, R.A., Ackley, S.F., Dieckmann, G.S., Gulliksen, B., Hoshiai, T., Legendre, L., Melnikov, I.A., Reeburgh, W.S., Spindler, M. and Sullivan, C.W. Ecology of sea ice biota. 1. Habitat, terminology, and methodology. Polar Biology 12: 417–427 (1992).

Krause, G. and Schauer, U. The expeditions ARKTIS XVI/1 and ARKTIS XVI/2 of the Research Vessel “Polarstern” in 2000. Berichte zur Polarforschung 389: 1–108 (2001).

Krembs, C., Gradinger, R. and Spindler, M. Implications of brine channel geometry and surface area for the interaction of sympagic organisms in Arctic sea ice. Journal of experimental marine Biology and Ecology 243: 55–80 (2000).

Lampitt, R.S., Noji, T.T. and Bodungen, B.V. What happens to zooplankton faecal pellets? Implications for material flux. Marine Biology 104: 15–23 (1990).

Lang, K. Monographie der Harpacticiden. Hakan Ohlsson Boktryckeri, Lund, Sweden (1948) 1682p

Leppäranta, M. and Manninen, T. The Brine and Gas Content of Sea Ice with Attention to Low Salinities and High Temperatures. Finnish Institute of Marine Research Internal Report 2: 1–14 (1988).

Martin, T. and Wadhams, P. Ice Fluxes within the Greenland Sea and their Variability. ESOP Scientific Report 1 (1996) 72–79.

Maykut, G.A. The ice environment. In Sea Ice Biota. R.A. Horner, ed., CRC Press, Boca Raton, Florida (1985) 21–82.

Montagna, P.A. and Carey, A.G. Jr. Distributional notes on Harpacticoida (Crustacea: Copepoda) collected from the Beaufort Sea (Arctic Ocean). Astarte 11: 117–122 (1978).

Schnack-Schiel, S.B., Dieckmann, G.S., Gradinger, R., Melnikov, I.A., Spindler, M. and Thomas, D.N. Meiofauna in sea ice of the Weddell Sea (Antarctica). Polar Biology 24: 724–728 (2001).

Swadling, K.M., McPhee, A.D. and McMinn, A. Spatial distribution of copepods in fast ice of eastern Antarctica. Polar Bioscience 13: 55–65 (2000).

Tremblay, C., Runge, J.A. and Legendre, L. Grazing and sedimentation of ice algae during and immediately after a bloom at the ice-water interface. Marine Ecology Progress Series 56: 291–300 (1989).

Verardo, D.J., Froelich, P.N. and McIntyre, A. Determination of organic carbon and nitrogen in marine sediments using the Carlo Erba Na-1500 analyzer. Deep-Sea Research I 37: 157–167 (1990).

Wadhams, P. Sea ice thickness distribution in Fram Strait. Nature 305: 108–111 (1983). Weissenberger, J. The environmental conditions in the brine channels of Antarctic sea-ice.

Berichte zur Polarforschung 111: 1–159 (1992). Werner, I. Ecological studies on the Arctic under-ice habitat - Colonization and processes

at the ice-water interface. Berichte des Sonderforschungsbereich 313 Univ. Kiel 70: 1–167 (1997).

Werner, I. Faecal pellet production by Arctic under-ice amphipods - transfer of organic matter through the ice/water interface. Hydrobiologia 426: 89–96 (2000).

Werner, I. and Martinez Arbizu, P. The sub-ice fauna of the Laptev Sea and the adjacent Arctic Ocean in summer 1995. Polar Biology 21: 71–79 (1999).

Werner, I., Auel, H. and Friedrich, C. Carnivorous feeding and respiration of the Arctic under-ice amphipod Gammarus wilkitzkii. Polar Biology 25: 523–530 (2002).