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Abundance, biomass and composition of the sea ice biota of the Greenland Sea pack ice
Deep-Sea Research II 46 (1999) 1457}1472
Abundance, biomass and composition of the sea ice biota of the Greenland Sea pack ice R. Gradinger*, C. Friedrich, M. Spindler Institute for Polar Ecology Kiel, Wischhofstr. 1}3, Geb. 12, D-24148 Kiel, Germany Received 2 February 1998; received in revised form 15 May 1998; accepted 4 September 1998
Abstract During two cruises to the Greenland Sea, we studied the abundance and biomass of the sea ice biota in summer and late autumn. The mean calculated biomass of the sympagic community was 0.2 g C m\ ice. Algae contributed on average 43% to total biomass, followed by bacteria (31%), heterotrophic #agellates (20%), and meiofauna (4%). Diatoms were the main primary producers (60% of total algal biomass), but #agellated cells contributed signi"cantly to the algal biomass. Among the meiofauna, ciliates, nematodes, acoel turbellarians and crustaceans were dominant. Calculated potential ingestion rates of meiofauna (0.6 g C m\ (120 d)\) are on the same order of magnitude as annual primary production estimates for Arctic multi-year sea ice. We therefore assume that grazing can control biomass accumulation of primary producers inside the sea ice. 1999 Elsevier Science Ltd. All rights reserved.
1. Introduction Sea ice covers between 7 (summer) and 14 (winter) 10 km of the Arctic Ocean (Maykut, 1985). The Arctic multi-year ice cover is generally thicker ('2 m) and, due to brine drainage, less saline than Antarctic sea ice (for a detailed comparison, see Spindler, 1990). Sea ice consists of a mixture of ice crystals and brine channels, the latter form a three-dimensional network with typical diameters of 200 lm within the ice matrix (Weissenberger et al., 1992). The brine salinity and the volume of the brine channels are dependent on the temperature and the salt content of the ice. A decrease in the ice temperature from !4 to !103C, for example, leads to growth
* Corresponding author. Tel.: #49-431-600-1236; fax: #49-431-600-1210. E-mail address: [email protected] (R. Gradinger) 0967-0645/99/$ - see front matter 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 9 9 ) 0 0 0 3 0 - 2
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of freshwater ice crystals and salt rejection and, thus, to an increase in brine salinity from 70 to 144 (Assur, 1958). Despite the extreme environmental conditions of temperature, salinity and light, a highly specialised so-called sympagic community has developed and adapted to live within the brine channel system. The succession of the sea ice algae is mainly controlled by abiotic parameters. The onset of algal growth in spring depends on the increase in available light following the dark polar winter. Sea ice, and especially the snow cover, reduce the incoming radiation due to their high albedo. Nevertheless, ice algae start growing under extremely low light, as soon as 2}10 lmol m\ s\ are exceeded (Horner and Schrader, 1982). The biomass built up by sea ice algae during the Arctic summer varies between 1 and 100 mg chl a m\ (Gradinger, 1995). Bacteria, proto- and metazoans, mostly smaller than 1 mm, also live in the brine channel system and feed on e.g., diatoms (Grainger and Mohammed, 1990). Ciliates, crustaceans, nematodes, rotifers and turbellarians comprise the dominant micro- and meiofauna in Arctic sea ice (Carey and Montagna, 1982; Cross, 1982; Gradinger et al., 1991; Grainger et al., 1985; Kern and Carey, 1983). Most studies of the sea ice community so far have been carried out in nearshore fast ice areas, where ice samples can be easily obtained from land-based stations. Research on drifting multi-year ice #oes requires expensive and highly sophisticated logistical support, e.g., ice-breaking ships or drifting ice camps. Thus, biological studies on Arctic pack ice systems are sparse (Melnikov, 1997), and only one biological study has focused on the sea-ice biota of the Greenland Sea (Gradinger et al., 1991,1992). These data, which were collected in April/May 1988 from a single ice #oe, suggested that the biomass and the community structure in Arctic drifting ice #oes are di!erent from those of coastal fast ice. Consequently, our present research within the European Subpolar Programme (ESOP) has focused on the quantitative description of the community structure of the Greenland Sea ice biota and its biomass in more detail. We could estimate the grazing impact of the sea ice meiofauna on the ice algal primary production. A combination of ice melting rates and our biomass data moreover, should allow the assessment of the carbon input through ice melting processes into the underlying water column of the Greenland Sea on an annual basis.
2. Material and methods All material was collected during two cruises with RV `Polarsterna into the Greenland Sea (Fig. 1). During the "rst expedition, ARK X/1 (6.7.1994}15.8.1994), we analysed biomass and composition of the sea ice community in the drifting pack ice. The main focus of the second cruise ARK XI/2 (22.9.1995}29.10.1995) was to study formation of new ice (Gradinger and IkaK valko, 1998), and therefore only algal biomass (chlorophyll a) was determined in older ice #oes. One (ARK XI/2) or two (ARK X/1) ice cores were taken at each ice #oe for physical and biological measurements using a 7.5 cm or 10 cm CRREL type ice auger. The temperature of the ice cores was measured at 5}10 cm vertical intervals immediately after coring with a Testo700 thermometer. Core 1 was melted for the #uorometrical
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Fig. 1. Station locations during the RV `Polarsterna expeditions ARK X/1 and ARK XI/2. Station number"day of the year.
determination of chlorophyll a (chl a) according to Evans and O'Reilly (1983), after "ltration on Whatman GF/F "lters. Salinity of the melted cores was determined with a WTW salinometer. Brine volumes were calculated according to Frankenstein and Garner (1967). Chl a concentrations of the brine were calculated assuming that all algae were located inside the brine channels. For the determination of organism abundance and biomass, core 2 (only during ARK X/1) was cut into 0.5}20 cm long sections, which were thawed in 0.2 lm pre-"ltered sea water (for details see Gradinger et al., 1991). A small subsample (5}50 ml) was "xed with formaldehyde (1% "nal concentration) and "ltered onto 0.2 lm Nuclepore "lters after DAPI staining (Porter and Feig, 1980). All "lters were kept frozen (!303C) for further analysis at the home laboratory. Bacterial and protist abundances were determined using a Zeiss epi#uorescence microscope equipped with UV and blue light excitation "lter sets, following the HELCOM (1989) recommendations. Cell sizes were measured with a New Porton Grid. Bacterial biomass was calculated using a mean carbon content of 0.03 pg C bacterium\ determined by Gradinger and Zhang (1997) for Arctic pack ice bacteria. Biomass of protists (except ciliates) was calculated following HELCOM (1989). Sea ice meiofauna concentrations were determined by either microscopy of live organisms onboard RV `Polarsterna or by counting of mostly Bouin-"xed (ciliates and acoel turbellaria) or formalin-"xed material in the home laboratory. For the determination of meiofauna biomass, di!erent approaches were used for each taxonomic group. Biomass of the sea-ice meiofauna was determined by size measurements of living or "xed organisms. The length and width of the organisms were measured using computer image analysis with a measurement error below 5%. Since specimens of each taxon were used for other purposes (e.g., species determination), only some
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specimens could be taken for biomass measurements. Therefore, in ice core samples, where the sizes of less than 90% of a taxon were measured, we used the median biomass of all measured specimens of the respective taxon. If more than 90% of the specimens of a taxon of one core could be measured, the missing values were treated as the median of the biomass of all specimens of the respective core. Finally, the biomass of each core was converted into biomass per square meter. Di!erent conversion factors were used for each taxonomic group: Nematodes: The wet weight (WW; lg) of nematodes (574 specimens) was calculated according to Riemann et al. (1990) with WW"0.9 ) p ) R ) ¸ ) 1.13;10\,
(1)
where R"1/2 width (lm) of the specimen, ¸"length (lm), 1.13"speci"c gravity (g cm\); (Wieser, 1960). The dry weight of nematodes was estimated as 22.5% of wet weight (average of the values of 20% and 25% given by Myers, 1967 and Wieser, 1960) and carbon content as constituting 40% of dry weight (Feller and Warwick, 1988). Rotifers: The sizes of only 15 specimens from six stations were measured since most of the rotifers contracted due to the "xation-process. The volume (<; lm) was calculated according to Ruttner}Kolisko (1977) with <"0.26 ) ¸ ) B,
(2)
where ¸"length without toes (lm), B"width (lm). As the rotifers were neutrally buoyant in seawater, the wet weight was calculated assuming a density of seawater of 1.028 (salinity"35 psu, 03C). The dry weight was estimated as 10% of the wet weight (Bottrell et al., 1976) and the carbon content as 8% of the biovolume (Beers and Stewart, 1970). In addition to these values, the biomass of four dominant rotifer species was calculated from literature data (Voigt and Koste, 1978; Chengalath, 1985). The median between these two data sets was taken as representative for all rotifers. Ciliates: Ciliates (77 specimens) were measured microscopically after Bouin-"xation and Protargol-staining. The volumes (<; lm) were calculated by the formula for a `#attened rotation ellipsoida (Auf dem Venne, 1994) with <"p ) ¸ ) B/12,
(3)
where ¸"length (lm), B"width (lm). To compensate for "xation-caused shrinking, the volumes were multiplied by 2.5 (Jerome et al., 1993; Auf dem Venne, 1994). The carbon-content was calculated as 8% of the cell volume (Beers and Stewart, 1970). Acoel turbellarians: The volume (<; nl) of acoels (196 specimens) was calculated according to Feller and Warwick (1988) with <"¸ ) B ) 550,
(4)
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where ¸"length (mm), B"width (mm). Wet weights were calculated by assuming a density of 1.13 (Wieser, 1960). Biomass was then calculated as described for the nematodes. Copepods: Copepod (122 specimens) volumes (<; nl) were calculated by the formula of Warwick and Gee (1984) with <"¸ ) B ) C,
(5)
where ¸"length incl. furca (mm), B"width (mm), C"speci"c conversion factor, depending on body shape: `Semi-cylindricala (Halectinosoma sp., Harpacticus sp. and Microsetella sp.) C"560 and `Pyriforma (other Copepoda) C"400). Wet weights, dry weights and carbon contents were calculated as described for the nematodes. Nauplii: The wet weight (WW; lg) of the nauplii (317 specimens) was calculated by a formula slightly modi"ed after Rachor (1975) with WW"¸ ) B ) C,
(6)
where ¸"length (mm), B"width (mm), C"conversion factor"360 lg mm\). Dry weight and carbon content were calculated as described for the nematodes. Based on the mean indivdual biomass of the sea-ice meiofauna taxa, we calculated the potential carbon ingestion rates of these organisms according to the allometric equations given by Moloney and Field (1989) for plankton organisms with I
"63 ) M\ , (7)
where I "potential maximum ingestion rate (d\), M"biomass of a single
organism. We assumed a Q value of 2 and calculated all rates for an ice temperature of } 13C, which is typical for Arctic sea ice in summer. For taxon-speci"c biomasses, M, we used the average values for each taxon determined in the analysed cores (Table 1).
Table 1 Biomass of meiofauna (medians) used for the calculation of potential ingestion rates (for details see Friedrich, 1997) Taxon
Individual biomass (ngC)
Nematodes Rotatoria Ciliates Acoel turbellaria Nauplii Copepods
129.6 23.3 10.7 391.8 21.7 656.3
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3. Results The distribution of organisms in the ice #oes showed very strong vertical gradients. Highest abundances of protists and metazoans as well as highest chlorophyll a (chl a) concentrations were always observed in the lowermost decimetres. Fig. 2 shows an example of the chl a distribution in an Arctic multi-year ice #oe collected at station 218 in the East Greenland Current in August 1994. Low-bulk salinities and relatively high temperatures are typical for Arctic summer sea ice. The calculated brine volume varied between 10 and 30% of the total ice volume. The Chl a pro"le clearly showed a well-developed bottom community with concentrations above 50 mg chl a m\ ice in the lowermost centimetres. The actual Chl a concentration within the brine channel system was far higher, exceeding 400 mg chl a m\ brine (Fig. 2). Ice temperatures (Fig. 3a) ranged between !1.6 and 0.93C in the Arctic summer. In autumn, ice was colder with values of !6.4}0.13C. The seasonal variation of the ice bulk salinity (Fig. 3b) was very small from 0.0 to 7.0 in summer to 0.0}9.2 in autumn. The relative brine volume (Fig. 3c) was lower in autumn 1995 than in summer 1994 due to lower temperature and salinity. The chlorophyll a concentrations (Fig. 4) in the brine were higher in autumn than in the summer with a maximum value of 2210 mg chl a m\ brine in the bottom 2 cm of one ice #oe. The integrated chlorophyll a concentrations (Fig. 5) ranged between 0.1 and 3.3 mg chl a m\ with a slightly, but not signi"cantly (p"0.1; Mann}Whitney U-Test) higher median of 2.0 mg chl a m\ in the autumn than in the summer (median of 1.2 mg chl a m\).
Fig. 2. Temperature, salinity, brine volume and algal biomass in an ice core from station 218.
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Fig. 3. Data range of observed (a) ice temperature, (b) salinity and (c) calculated brine volumes for all pack ice samples during ARK X/1 (n"258) and ARK XI/2 (n"195). In the box plots the total data range and the 25}75% quartile range are shown. Single data points were marked as outliers, when they exceeded a value < of <"UQ#1.5 ) IQD or <"LQ!1.7 ) IQD (LQ"lower quartile, UQ"upper quartile, IQD"interquartile distance).
The major primary producers inside the sea ice were pennate diatoms, but we also observed considerable concentrations of #agellates (e.g., Fig. 6). Ciliates and metazoans were closely related to the vertical distribution of the algae with their highest concentrations in the lowermost 2 cm, although metazoans also occurred more than 1 m above the bottom of the ice #oes. On average (means), the sympagic summer
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Fig. 4. Calculated algal biomass in the brine of all ice samples during ARK X/1 (n"258) and ARK XI/2 (n"195). For explanation of box plots see Fig. 3.
community (integrated over entire ice thickness) consisted of 20.5;10 bacteria, 683;10 pennate diatoms, 65;10 centric diatoms, 799;10 phototrophic and 882;10 heterotrophic #agellates m\ ice. Sea-ice meiofauna mainly consisted of ciliates (83.6;10 m\), nematodes (21.6;10 m\), acoel turbellarians (5.5;10 m\), copepods (2.4;10 m\), and rotifers (2.2;10 m\). Based on the microscopical analyses of the ice cores, we calculated the organic carbon concentration within the sea ice of the Greenland Sea (Fig. 7). Integrated mean biomass of all sea ice organisms added up to 195.6 mg C m\ sea ice. Bacteria contributed the largest fraction of organic carbon (31%) followed by pennate diatoms (26%), heterotrophic (20%) and phototrophic (17%) #agellates. The meiofauna contributed only a minor fraction to total biomass (3.7%). Nematodes (1.5%), acoel turbellarians (0.9%) and copepods (0.8%) were the dominant metazoa in the ice cores. The mean ratio of heterotrophic to phototrophic biomass was 2.0. Relative to the phototrophic biomass, which was set to 1, bacterial biomass was 1.2$0.5 (standard error), for protozoa 0.6$0.1 and for meiofauna 0.2$0.1.
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Fig. 5. Integrated algal biomass in pack ice from the Greenland Sea (this study), the central Arctic Ocean (Gradinger, unpubl. data) and three fast ice regions (Cota et al., 1991; maximum levels were provided). For explanation of box plots see Fig. 3. Horizontal lines inside the boxes of the pack ice data indicate median values.
Fig. 6. Biomass of bacteria, pennate diatoms, photo- and heterotrophic protists and abundance of sea ice meiofauna in an ice core from station 216.
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Fig. 7. Integrated biomass of the sea-ice biota (n"6 ice cores) in the Greenland Sea in summer 1994. For explanation of box plots see Fig. 3. Horizontal lines inside the boxes indicate median values.
Martin and Wadhams (1996) provided the annual ice #ux rates for the Greenland Sea in 1994. Their data showed that 530;10 m sea ice melt between 793N and 703N. This melt leads to a release of sympagic biomass of roughly 0.104 Tg C y\, if we assume a biomass of the sympagic community of 0.2 g C m\ ice (Fig. 7). Most of the ice melt (71%) takes place between 763N and 753N, which leads to an input of about 0.074 Tg C y\ from the ice into the pelagic realm in this area. The carbon-based grazing model of Moloney and Field (1989) allowed us to estimate the potential grazing impact of sea ice meiofauna (Fig. 8). The calculated weight speci"c ingestion rates ranged between 1.44 d\ (ciliates) and 0.52 d\ (copepods) at a temperature of !13C. The total meiofauna community had a potential daily ingestion rate between 2.1 and 11.2 mg C m\ d\ with an average of 5.5 mg C m\ d\ at the investigated stations. For further calculations, we assumed that this activity only occurs during the Arctic productive summer phase (120 days) leading to a total potential ingestion of 656 mg C m\ (120 d)\.
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Fig. 8. Potential maximum ingestion rates of sea-ice meiofauna (n"6 ice cores) in the Greenland Sea in summer 1994. For explanation of box plots see Fig. 3. Horizontal lines inside the boxes indicate median values.
4. Discussion Major regions of ice formation are located on the Russian shelf areas, i.e., the Kara Sea, Laptev Sea and East Siberian Sea (Carmack and Swift, 1990). From these areas, the ice #oes are transported by the Transpolar Drift through the central Arctic Ocean until they enter the Greenland Sea through the Fram Strait and subsequently melt. About 10% of the sea ice in the Arctic basin is exported each year through Fram Strait into the Greenland Sea (Maykut, 1985). Hence, our sampling took place in the major export area of multi-year drift ice from the central Arctic. Our results may be representative for the ice conditions within the Arctic basin; the integrated algal biomass data from ARK X/1 and ARK XI/2 "t into the data range obtained during the Polarstern summer expedition ARK VIII/3 in the central Arctic (for cruise details see FuK tterer, 1991), where we sampled 47 ice #oes up to 903N (Fig. 5; Gradinger, unpubl. data). Published data from coastal fast ice areas (Cota et al., 1991) are orders of magnitude higher, indicating di!erent growth conditions for algae in di!erent types of sea ice. The lower biomass in drifting pack ice can be attributed to lower nutrient supply, di!erent physical parameters (ice temperature, brine salinity, radiation) or biological interactions (grazing and growth rates). Nitrate concentrations in ice cores during ARK X/1 were below the detection limit in most parts of the ice ((0.1 mmol m\; Gradinger unpubl. data) and only slightly higher close to the bottom of the ice #oes. Thus, limited nitrogen resources in ice #oes may limit algal development in the #oe interiors, such as in the coastal sea ice of the Canadian Arctic (Cota et al., 1987; Demers et al., 1989). Therefore, the exchange of dissolved inorganic nutrients between sea-ice brine channels and the pelagic realm in#uences the ice algal primary production (Cota et al., 1987; Gradinger et al., 1992). Besides nutrient supply,
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the marked seasonal variation of environmental factors a!ects the distribution and total biomass accumulation of ice organisms. Arctic ice diatoms are, however, euryhaline and can grow over a wide range of salinities (Grant and Horner, 1976; Zhang et al., in press), Antarctic ice diatoms even at salinities of 95 and !5.53C temperature (Bartsch, 1989). Antarctic and Arctic sympagic copepods have much higher salinity tolerances than pelagic ones (Dahms et al., 1990; Grainger and Mohammed, 1990). Our studies (Friedrich, 1997) and that by Grainger and Mohammed (1990) show that Arctic sea-ice metazoans are euryhaline and not restricted in their distribution inside the ice by temperature or brine salinity during the Arctic summer. They even occur more than 1 m above the underside of the ice #oes (e.g., Fig. 6). However, winter conditions with ice temperatures below !103C and brine salinities above 140 are lethal at least for acoel turbellarians and copepods (Friedrich 1997). Thus, winter survival probably causes, to a large extent, the distribution patterns that are typical for the Arctic bottom-ice communities we observed in summer and autumn. To validate this hypothesis, sea-ice data from early spring and the winter period are needed. The traditional view of the sympagic algal community, summarised by Poulin (1990), has diatoms as the main primary producers in Arctic sea ice. Our study is the "rst that attempts to evaluate the contribution of small #agellated taxa to total ice algal biomass, based on the analysis of entire sea ice cores. The #agellates contribute signi"cantly to overall biodiversity (IkaK valko and Gradinger, 1997). Phototrophic protists other than diatoms provided an average of 40% to the entire algal biomass and were even dominant in some cores. Autecological studies on sea-ice algae have been conducted only with sympagic diatoms from the Arctic and Antarctic (e.g., Bartsch, 1989; Gleitz et al., 1996), and it is questionable if these results can be extrapolated to #agellates. The high abundance of heterotrophic #agellates further increases the diversity of the sympagic community and indicates a microbial food web inside the ice, as already proposed by Laurion et al. (1995). The ice meiofauna composition was similar to that in early spring (Gradinger et al., 1991), with nematodes, acoel turbellarians and ciliates as most abundant taxa. Meroplanktic larvae of benthic polychaetes and molluscs, which inhabit coastal fast ice (Carey and Montagna, 1982), were never observed in any of the ice cores of the Greenland Sea. The overall composition of the sympagic community was very similar to results from oceanic pelagic habitats, where the ratio of heterotrophic (bacteria#protozoa# metazoa) to phototrophic biomass is close to 1.9 (Gasol et al., 1997). Consequently, also in Arctic sea ice we found an `inverted trophic pyramida. Gasol et al. (1997) proposed that such communities develop due to high algal biomass-speci"c activities. In the case of ice algae, typical P ratios are below 0.4 mg C mg C\ d\ (Cota and Smith, 1991), which is close to values obtained for coastal phytoplankton populations. Consequently, we assume that algal growth parameters alone cannot be responsible for the observed trophic pyramid in the sea ice. Further factors in#uence the trophic structure of the sea ice food web. The delicate structure of the brine channels leads, for example, to a spatial exclusion of larger predators as can be seen from their relatively low contribution to overall biomass compared to pelagic data from both oceanic and coastal locations.
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Present knowledge on grazing as a structuring factor for the development of sea-ice biota is still very poor and basic. Laurion et al. (1995) gave "rst estimates on grazing rates of heterotrophic protists on ice bacteria, which are similar to rates in other marine aquatic habitats. To date, no estimate exists for the impact of the sea-ice meiofauna. Our grazing model suggests, as a rough estimate, a potential carbon ingestion by meiofauna of about 650 mg C m\ during the productive Arctic summer (120 days). Legendre et al. (1992) proposed an annual primary production by Arctic multi-year sea-ice algae of about 600 mg C m\. Thus, the carbon ingestion by meiofauna is on the same order of magnitude as the primary production. It follows that, in addition to limited nutrient supply, grazing by sea-ice meiofauna may control the accumulation of organic biomass in the sea ice. This result is in contrast to that of, e.g., Meguro et al. (1967), who suggested that there was no grazing in the ice. Estimates on the role of ice metazoa from coastal areas are not available. We noticed the ingestion of diatoms by the acoel turbellarians as did Grainger and Hsiao (1990), but we did not observe any food uptake by nematodes. The available food concentration inside the brine channels is 1}5 orders of magnitude higher than typical algal biomass in the water column of ice-covered Arctic waters or in marginal ice zone blooms (Gradinger and Baumann, 1991). Grazing might thus be prolonged into the dark season so that the annual grazing rate is higher than our estimate for 120 days. Furthermore, we did not include protists other than ciliates in our calculations because we assumed that they are primarily bacterivorous. However, some species such as heterotrophic euglenophytes or dino#agellates are known to feed on pennate diatoms (Buck et al., 1990; IkaK valko and Gradinger, 1997), leading to even higher potential ingestion. The discrepancy between previous primary production estimates for Arctic multi-year ice #oes (Legendre et al., 1992) and our calculations of potential grazing e!ects, as well as in-situ algal biomass both for the inside of the sea ice and the top of the #oes (Gradinger and NuK rnberg, 1996), present further evidence to the statement of Wheeler et al. (1996) that primary production within the icecovered Arctic Ocean is at least one order of magnitude greater than previously assumed. The Greenland Sea is the major melting area for sea ice leaving the central Arctic Ocean by the Transpolar Drift. Thus, the entire ice biota is released into the water column there and may either contribute to pelagic production or sink to the sea #oor. We estimated an annual release of organic biomass of about 0.1 Tg C y\ from melting ice into the water column between 79 and 703N for 1994. Compared with the annual new production by phytoplankton (56 g C m\ y\; Noji et al., 1996), the input of carbon from the ice to the water column is of minor importance for the organic carbon cycle of the Greenland Sea. Nevertheless, the release may have considerable in#uence on the pelagic and benthic realms. The released algae may either initiate the spring algal plankton bloom (Smith and Sakshaug, 1990) or they may sink to the sea #oor and serve as an episodic and "rst food pulse for benthic organisms before pelagic production begins (Carey, 1987). Future models on the carbon budget of ice covered areas such as that by Slagstad et al. (1996) should therefore include a coupled ice-pelagic component.
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Acknowledgements The helpfulness of the crew of the RV Polarstern is gratefully acknowledged. We would like to thank our colleagues for assistance during the expeditions and fruitful discussions at sea and in the home labs. This study was supported by the Commission of the European Community under contract MAS2-CT93-0057 of the MAST-II programme. The Deutsche Forschungsgemeinschaft (DFG Gr 1405/1-1) provided the microscopical equipment used by RG.
References Assur, A., 1958. Composition of sea ice and its tensile strength. National Research Council Publications 598, 106}138. Auf dem Venne, H., 1994. Zur Verbreitung und oK kologischen Bedeutung planktischer Ciliaten in zwei verschiedenen Meeresgebieten: GroK nlandsee und Ostsee. Berichte aus dem Institut fuK r Meereskunde Kiel 262, 1}160. Bartsch, A., 1989. Die Eisalgen#ora des Weddellmeeres (Antarktis): Artenzusammensetzung und Biomasse sowie OG kophysiologie ausgewaK hlter Arten. Berichte zur Polarforschung 63, 1}110. Beers, J.R., Stewart, G.L., Part VI: Numerical abundance and estimated biomass of microzooplankton. In: Strickland, J.D.H. (Eds.), The ecology of the plankton o! La Jolla, California, in the period April through September, 1967. Bulletin Scripps Institution of Oceanography, Vol. 17, pp. 67}87. Bottrell, H.H., Duncan, A., Gliwicz, Z.M., Grygierek, E., Herzig, A., Hillbricht-Ilkowska, A., Kurasawa, H., Larsson, P., Weglenska, T., 1976. A review of some problems in zooplankton production studies. Norwegian Journal Zoology 24, 419}456. Buck, K.R., Bolt, P.A., Garrison, D.L., 1990. Phagotrophy and fecal pellet production by an athecate dino#agellate in Antarctic sea ice. Marine Ecology Progress Series 60, 75}84. Carey, A.G., 1987. Particle #ux beneath fast ice in the shallow southwestern Beaufort Sea, Arctic Ocean. Marine Ecology Progress Series 40, 247}257. Carey, A.G., Montagna, P.A., 1982. Arctic sea ice faunal assemblage: First approach to description and source of the underice meiofauna. Marine Ecology Progress Series 8, 1}8. Carmack, E.C., Swift, J.H., 1990. Some aspects of the large-scale physical oceanography of the Arctic Ocean in#uencing biological distributions. In: Medlin, L.K., Priddle, J. (Eds.), Polar marine diatoms. British Antarctic Survey, Cambridge, pp. 35}46. Chengalath, R., 1985. The rotifera of the Canadian Arctic sea ice, with the description of a new species. Canadian Journal of Zoology 63, 2212}2218. Cota, G.F., Legendre, L., Gosselin, M., Ingram, R.G., 1991. Ecology of bottom ice algae: I. Environmental controls and variabilty. Journal of Marine Systems 2, 257}278. Cota, G.F., Prinsenberg, S.J., Bennett, E.B., Loder, J.W., Lewis, M.R., Anning, J.L., Watson, N.H.F., Harris, L.R., 1987. Nutrient #uxes during extended blooms of Arctic ice algae. Journal of Geophysical Research 92, 1951}1962. Cota, G.F., Smith, R.E.H., 1991. Ecology of bottom ice algae: III. Comparitive physiology. Journal Marine Systems 2, 297}315. Cross, W.E., 1982. Under-ice biota at the Pond Inlet ice edge and in adjacent fast ice areas during spring. Arctic 35, 13}27. Dahms, H.-U., Bergmans, M., Schminke, H.K., 1990. Distribution and adaptations of sea ice inhabiting Harpacticoida (Crustacea, Copepoda) of the Weddell Sea (Antarctica). Marine Ecology 11, 207}226. Demers, S., Legendre, L., Maestrini, S., Rochet, M., Ingram, R., 1989. Nitrogenous nutrition of sea-ice microalgae. Polar Biology 9, 377}383. Evans, C.A., O'Reilly, J.E., 1983. A handbook for the measurement of chlorophyll a in netplankton and nanoplankton. SCAR/BIOMASS Handbook, vol. 9, pp. 1}44.
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Feller, R.J., Warwick, R.M., 1988. 13. Energetics. In: Higgins, R.P., Thiel, H. (Eds.), Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp. 181}196. Frankenstein, G., Garner, R., 1967. Equations for determining the brine volume of sea ice from !0.53C to !22.93C. Journal of Glaciology 6, 943}944. Friedrich, C., 1997. Ecological investigations on the fauna of the Arctic sea-ice. Berichte zur Polarforschung 246, 1}211. FuK tterer, D.K. (with contributions of the participants), 1991. ARCTIC '91: Die Expedition ARK-VIII/3 mit FS `Polarsterna 1991. Berichte zur Polarforschung 107, 1-267. Gasol, J.M., del Giorgio, P.A., Duarte, C.M., 1997. Biomass distribution in marine planktonic communities. Limnolology and Oceanography 42, 1353}1363. Gleitz, M., Kukert, H., Riebesell, U., Dieckmann, G.S., 1996. Carbon acquisition and growth of Antarctic sea-ice diatoms in closed bottle incubations. Marine Ecology Progress Series 135, 169}177. Gradinger, R., 1995. Climate change and biological oceanography of the Arctic Ocean. Philosophical Transactions of the Royal Society London A 352, 277}286. Gradinger, R.R., Baumann, M.E.M., 1991. Distribution of phytoplankton communities in relation to the large-scale hydrographical regime in the Fram Strait. Marine Biology 111, 311}321. Gradinger, R., NuK rnberg, D., 1996. Snow algal communities on Arctic pack ice #oes dominated by Chlamydomonas nivalis (Bauer) Wille. Proceedings of the NIPR Symposium on Polar Biology, vol. 9, pp. 35}43. Gradinger, R., Spindler, M., Henschel, D., 1991. Development of Arctic sea-ice organisms under graded snow cover. Polar Research 10, 295}307. Gradinger, R., Spindler, M., Weissenberger, J., 1992. On the structure and development of Arctic pack ice communities in Fram Strait: a multivariate approach. Polar Biology 12, 727}733. Gradinger, R., IkaK valko, J., 1998. Organisms incorporation into newly forming Arctic sea ice in the Greenland Sea. Journal of Plankton Research 20, 871}886. Gradinger, R., Zhang, Q., 1997. Vertical distribution of bacteria in Arctic sea ice from the Barents and Laptev Seas. Polar Biology 17, 448}454. Grainger, E.H., Hsiao, S.I.C., 1990. Trophic relationships of the sea ice meiofauna in Frobisher Bay, Arctic Canada. Polar Biology 10, 283}292. Grainger, E.H., Mohammed, A.A., Lovrity, J.E., 1985. The sea ice fauna of Frobisher Bay, Arctic Canada. Arctic 38, 23}30. Grainger, E.H., Mohammed, A.A., 1990. High salinity tolerance in sea-ice copepods. Ophelia 31, 177}185. Grant, W.S., Horner, R.A., 1976. Growth responses to salinity variation in four Arctic ice diatoms. Journal of Phycology 12, 180}185. HELCOM, 1989. Guidelines for the Baltic monitoring programme for the third stage. Part D. Biological determinands. Finnish Governmental Printing Centre, Helsinki, 161 pp. Horner, R., Schrader, G.C., 1982. Relative contribution of ice algae, phytoplankton, and benthic microalgae to primary production in nearshore regions of the Beaufort Sea. Arctic 35, 485}503. IkaK valko, J., Gradinger, R., 1997. Flagellates and heliozoans in the Greenland Sea ice studied alive using light microscopy. Polar Biology 17, 473}481. Jerome, C.A., Montagnes, D.J.S., Taylor, F.J.R., 1993. The e!ect of the Quantitative Protargol Stain and Lugol's and Bouin's "xatives on cell size: a more accurate estimate of ciliate species biomass. Journal Eukaryotic Microbiology 40, 254}259. Kern, J.C., Carey, A.G., 1983. The faunal assemblage inhabiting seasonal sea ice in the nearshore Arctic Ocean with emphasis on copepods. Marine Ecology Progress Series 10, 159}167. Laurion, I., Demers, S., Vezina, A.F., 1995. The microbial food web associated with the ice algal assemblage: Biomass and bacterivory of nano#agellate protozoans in Resolute Passage (High Canadian Arctic). Marine Ecology Progress Series 120, 77}87. Legendre, L., Ackley, S.F., Dieckmann, G.S., Gulliksen, B., Horner, R., Hoshiai, T., Melnikov, I.A., Reeburgh, W.S., Spindler, M., Sullivan, C.W., 1992. Ecology of sea-ice biota. 2. Global signi"cance. Polar Biology 12, 429}444. Martin, T., Wadhams, P., 1996. Ice #uxes within the Greenland Sea and their variabiliy. ESOP Scienti"c Report 1, 72}79.
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Maykut, G.A., 1985. The ice environment. In: Horner, R. (Ed.), Sea-ice biota. CRC Press, Boca Raton, pp. 21}82. Meguro, H., Ito, K., Fukushima, H., 1967. Ice #ora (bottom type): a mechanism of primary production in polar seas and the growth of diatoms in sea ice. Arctic 20, 114}133. Melnikov, I., 1997. The Arctic sea-ice ecosystem. Gordon and Breach, Amsterdam, 204 pp. Moloney, C.L., Field, J.G., 1989. General allometric equations for rates of nutrient uptake, ingestion, and respiration in plankton organisms. Limnology and Oceanography 34, 1290}1299. Myers, R.F., 1967. Osmoregulation in Pangrellus redivivus and Aphelenchus avanae. Nematologica 12, 579}586. Noji, T.T., Rey, F., Miller, L., B+rsheim, K.Y., Hirche, H.-J., Urban-Rich, J., 1996. Plankton dynamics and sedimentation. ESOP Report, vol. 2, pp. 540}554. Porter, K.G., Feig, Y.S., 1980. The use of DAPI for identifying and counting aquatic micro#ora. Limnology and Oceanography 25, 943}948. Poulin, M., 1990. Ice diatoms: the Arctic. In: Medlin, L.K., Priddle, J. (Eds.), Polar marine diatoms. British Antarctic Survey, Cambridge, pp. 15}18. Rachor, E., 1975. Quantitative Untersuchungen uK ber das Meiobenthos der nordostatlantischen Tiefsee. `Meteora-Forschungs-Ergebnisse. Reihe D 21, 1}10. Riemann, F., Ernst, W., Ernst, R., 1990. Acetate uptake from ambient water by the free-living marine nematode Adoncholaimus thalassophygas. Marine Biology 104, 453}457. Ruttner-Kolisko, A., 1977. Suggestions for biomass calculation of plankton rotifers. Archiv fuK r Hydrobiologie 8, 71}76. Slagstad, D., Downing, K., Carlotti, F., Hirche, H.-J., 1999. Modelling the carbon export and air}sea #ux of CO in the Greenland Sea. Deep-Sea Research II 46, 1511}1530. Smith Jr, W.O., Sakshaug, E., 1990. Polar phytoplankton. In: Smith Jr, W.O. (Ed.), Polar oceanography. Part B. Chemistry, biology and geology. Academic Press, San Diego, pp. 477}525. Spindler, M., 1990. A comparison of Arctic and Antarctic sea ice and the e!ects of di!erent properties on sea-ice biota. In: Bleil, U., Thiede, J. (Eds.), Geological history of the polar oceans: Arctic versus Antarctic. Kluwer Academic Publishers, Dordrecht, pp. 173}186. Voigt, M., Koste, W., 1978. Rotatoria. Die RaK dertiere Mitteleuropas. Gebr. Borntraeger, Berlin., vol. I, 673 pp. Warwick, R.M., Gee, J.M., 1984. Community structure of estuarine meiobenthos. Marine Ecology Progress Series 18, 97}111. Weissenberger, J., Dieckmann, G., Gradinger, R., Spindler, M., 1992. Sea ice: A cast technique to examine and analyze brine pockets and channel structure. Limnology and Oceanography 37, 179}183. Wheeler, P.A., Gosselin, M., Sherr, E., Thibault, D., Kirchman, D.L., Benner, R., Whitledge, T.E., 1996. Active cycling of organic carbon in the central Arctic Ocean. Nature 380, 697}699. Wieser, W., 1960. Benthic studies in Buzzards Bay. II. The meiofauna. Limnology and Oceanography 5, 121}137. Zhang Q., Gradinger, R., Spindler, M. Experimental study on the e!ect of salinity on growth rates of Arctic sea-ice algae from the Greenland Sea. Boreal Environmental Research, in press.
Abundance, biomass and composition of the sea ice biota of the Greenland Sea pack ice R. Gradinger*, C. Friedrich, M. Spindler Institute for Polar Ecology Kiel, Wischhofstr. 1}3, Geb. 12, D-24148 Kiel, Germany Received 2 February 1998; received in revised form 15 May 1998; accepted 4 September 1998
Abstract During two cruises to the Greenland Sea, we studied the abundance and biomass of the sea ice biota in summer and late autumn. The mean calculated biomass of the sympagic community was 0.2 g C m\ ice. Algae contributed on average 43% to total biomass, followed by bacteria (31%), heterotrophic #agellates (20%), and meiofauna (4%). Diatoms were the main primary producers (60% of total algal biomass), but #agellated cells contributed signi"cantly to the algal biomass. Among the meiofauna, ciliates, nematodes, acoel turbellarians and crustaceans were dominant. Calculated potential ingestion rates of meiofauna (0.6 g C m\ (120 d)\) are on the same order of magnitude as annual primary production estimates for Arctic multi-year sea ice. We therefore assume that grazing can control biomass accumulation of primary producers inside the sea ice. 1999 Elsevier Science Ltd. All rights reserved.
1. Introduction Sea ice covers between 7 (summer) and 14 (winter) 10 km of the Arctic Ocean (Maykut, 1985). The Arctic multi-year ice cover is generally thicker ('2 m) and, due to brine drainage, less saline than Antarctic sea ice (for a detailed comparison, see Spindler, 1990). Sea ice consists of a mixture of ice crystals and brine channels, the latter form a three-dimensional network with typical diameters of 200 lm within the ice matrix (Weissenberger et al., 1992). The brine salinity and the volume of the brine channels are dependent on the temperature and the salt content of the ice. A decrease in the ice temperature from !4 to !103C, for example, leads to growth
* Corresponding author. Tel.: #49-431-600-1236; fax: #49-431-600-1210. E-mail address: [email protected] (R. Gradinger) 0967-0645/99/$ - see front matter 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 9 9 ) 0 0 0 3 0 - 2
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of freshwater ice crystals and salt rejection and, thus, to an increase in brine salinity from 70 to 144 (Assur, 1958). Despite the extreme environmental conditions of temperature, salinity and light, a highly specialised so-called sympagic community has developed and adapted to live within the brine channel system. The succession of the sea ice algae is mainly controlled by abiotic parameters. The onset of algal growth in spring depends on the increase in available light following the dark polar winter. Sea ice, and especially the snow cover, reduce the incoming radiation due to their high albedo. Nevertheless, ice algae start growing under extremely low light, as soon as 2}10 lmol m\ s\ are exceeded (Horner and Schrader, 1982). The biomass built up by sea ice algae during the Arctic summer varies between 1 and 100 mg chl a m\ (Gradinger, 1995). Bacteria, proto- and metazoans, mostly smaller than 1 mm, also live in the brine channel system and feed on e.g., diatoms (Grainger and Mohammed, 1990). Ciliates, crustaceans, nematodes, rotifers and turbellarians comprise the dominant micro- and meiofauna in Arctic sea ice (Carey and Montagna, 1982; Cross, 1982; Gradinger et al., 1991; Grainger et al., 1985; Kern and Carey, 1983). Most studies of the sea ice community so far have been carried out in nearshore fast ice areas, where ice samples can be easily obtained from land-based stations. Research on drifting multi-year ice #oes requires expensive and highly sophisticated logistical support, e.g., ice-breaking ships or drifting ice camps. Thus, biological studies on Arctic pack ice systems are sparse (Melnikov, 1997), and only one biological study has focused on the sea-ice biota of the Greenland Sea (Gradinger et al., 1991,1992). These data, which were collected in April/May 1988 from a single ice #oe, suggested that the biomass and the community structure in Arctic drifting ice #oes are di!erent from those of coastal fast ice. Consequently, our present research within the European Subpolar Programme (ESOP) has focused on the quantitative description of the community structure of the Greenland Sea ice biota and its biomass in more detail. We could estimate the grazing impact of the sea ice meiofauna on the ice algal primary production. A combination of ice melting rates and our biomass data moreover, should allow the assessment of the carbon input through ice melting processes into the underlying water column of the Greenland Sea on an annual basis.
2. Material and methods All material was collected during two cruises with RV `Polarsterna into the Greenland Sea (Fig. 1). During the "rst expedition, ARK X/1 (6.7.1994}15.8.1994), we analysed biomass and composition of the sea ice community in the drifting pack ice. The main focus of the second cruise ARK XI/2 (22.9.1995}29.10.1995) was to study formation of new ice (Gradinger and IkaK valko, 1998), and therefore only algal biomass (chlorophyll a) was determined in older ice #oes. One (ARK XI/2) or two (ARK X/1) ice cores were taken at each ice #oe for physical and biological measurements using a 7.5 cm or 10 cm CRREL type ice auger. The temperature of the ice cores was measured at 5}10 cm vertical intervals immediately after coring with a Testo700 thermometer. Core 1 was melted for the #uorometrical
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Fig. 1. Station locations during the RV `Polarsterna expeditions ARK X/1 and ARK XI/2. Station number"day of the year.
determination of chlorophyll a (chl a) according to Evans and O'Reilly (1983), after "ltration on Whatman GF/F "lters. Salinity of the melted cores was determined with a WTW salinometer. Brine volumes were calculated according to Frankenstein and Garner (1967). Chl a concentrations of the brine were calculated assuming that all algae were located inside the brine channels. For the determination of organism abundance and biomass, core 2 (only during ARK X/1) was cut into 0.5}20 cm long sections, which were thawed in 0.2 lm pre-"ltered sea water (for details see Gradinger et al., 1991). A small subsample (5}50 ml) was "xed with formaldehyde (1% "nal concentration) and "ltered onto 0.2 lm Nuclepore "lters after DAPI staining (Porter and Feig, 1980). All "lters were kept frozen (!303C) for further analysis at the home laboratory. Bacterial and protist abundances were determined using a Zeiss epi#uorescence microscope equipped with UV and blue light excitation "lter sets, following the HELCOM (1989) recommendations. Cell sizes were measured with a New Porton Grid. Bacterial biomass was calculated using a mean carbon content of 0.03 pg C bacterium\ determined by Gradinger and Zhang (1997) for Arctic pack ice bacteria. Biomass of protists (except ciliates) was calculated following HELCOM (1989). Sea ice meiofauna concentrations were determined by either microscopy of live organisms onboard RV `Polarsterna or by counting of mostly Bouin-"xed (ciliates and acoel turbellaria) or formalin-"xed material in the home laboratory. For the determination of meiofauna biomass, di!erent approaches were used for each taxonomic group. Biomass of the sea-ice meiofauna was determined by size measurements of living or "xed organisms. The length and width of the organisms were measured using computer image analysis with a measurement error below 5%. Since specimens of each taxon were used for other purposes (e.g., species determination), only some
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specimens could be taken for biomass measurements. Therefore, in ice core samples, where the sizes of less than 90% of a taxon were measured, we used the median biomass of all measured specimens of the respective taxon. If more than 90% of the specimens of a taxon of one core could be measured, the missing values were treated as the median of the biomass of all specimens of the respective core. Finally, the biomass of each core was converted into biomass per square meter. Di!erent conversion factors were used for each taxonomic group: Nematodes: The wet weight (WW; lg) of nematodes (574 specimens) was calculated according to Riemann et al. (1990) with WW"0.9 ) p ) R ) ¸ ) 1.13;10\,
(1)
where R"1/2 width (lm) of the specimen, ¸"length (lm), 1.13"speci"c gravity (g cm\); (Wieser, 1960). The dry weight of nematodes was estimated as 22.5% of wet weight (average of the values of 20% and 25% given by Myers, 1967 and Wieser, 1960) and carbon content as constituting 40% of dry weight (Feller and Warwick, 1988). Rotifers: The sizes of only 15 specimens from six stations were measured since most of the rotifers contracted due to the "xation-process. The volume (<; lm) was calculated according to Ruttner}Kolisko (1977) with <"0.26 ) ¸ ) B,
(2)
where ¸"length without toes (lm), B"width (lm). As the rotifers were neutrally buoyant in seawater, the wet weight was calculated assuming a density of seawater of 1.028 (salinity"35 psu, 03C). The dry weight was estimated as 10% of the wet weight (Bottrell et al., 1976) and the carbon content as 8% of the biovolume (Beers and Stewart, 1970). In addition to these values, the biomass of four dominant rotifer species was calculated from literature data (Voigt and Koste, 1978; Chengalath, 1985). The median between these two data sets was taken as representative for all rotifers. Ciliates: Ciliates (77 specimens) were measured microscopically after Bouin-"xation and Protargol-staining. The volumes (<; lm) were calculated by the formula for a `#attened rotation ellipsoida (Auf dem Venne, 1994) with <"p ) ¸ ) B/12,
(3)
where ¸"length (lm), B"width (lm). To compensate for "xation-caused shrinking, the volumes were multiplied by 2.5 (Jerome et al., 1993; Auf dem Venne, 1994). The carbon-content was calculated as 8% of the cell volume (Beers and Stewart, 1970). Acoel turbellarians: The volume (<; nl) of acoels (196 specimens) was calculated according to Feller and Warwick (1988) with <"¸ ) B ) 550,
(4)
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1461
where ¸"length (mm), B"width (mm). Wet weights were calculated by assuming a density of 1.13 (Wieser, 1960). Biomass was then calculated as described for the nematodes. Copepods: Copepod (122 specimens) volumes (<; nl) were calculated by the formula of Warwick and Gee (1984) with <"¸ ) B ) C,
(5)
where ¸"length incl. furca (mm), B"width (mm), C"speci"c conversion factor, depending on body shape: `Semi-cylindricala (Halectinosoma sp., Harpacticus sp. and Microsetella sp.) C"560 and `Pyriforma (other Copepoda) C"400). Wet weights, dry weights and carbon contents were calculated as described for the nematodes. Nauplii: The wet weight (WW; lg) of the nauplii (317 specimens) was calculated by a formula slightly modi"ed after Rachor (1975) with WW"¸ ) B ) C,
(6)
where ¸"length (mm), B"width (mm), C"conversion factor"360 lg mm\). Dry weight and carbon content were calculated as described for the nematodes. Based on the mean indivdual biomass of the sea-ice meiofauna taxa, we calculated the potential carbon ingestion rates of these organisms according to the allometric equations given by Moloney and Field (1989) for plankton organisms with I
"63 ) M\ , (7)
where I "potential maximum ingestion rate (d\), M"biomass of a single
organism. We assumed a Q value of 2 and calculated all rates for an ice temperature of } 13C, which is typical for Arctic sea ice in summer. For taxon-speci"c biomasses, M, we used the average values for each taxon determined in the analysed cores (Table 1).
Table 1 Biomass of meiofauna (medians) used for the calculation of potential ingestion rates (for details see Friedrich, 1997) Taxon
Individual biomass (ngC)
Nematodes Rotatoria Ciliates Acoel turbellaria Nauplii Copepods
129.6 23.3 10.7 391.8 21.7 656.3
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3. Results The distribution of organisms in the ice #oes showed very strong vertical gradients. Highest abundances of protists and metazoans as well as highest chlorophyll a (chl a) concentrations were always observed in the lowermost decimetres. Fig. 2 shows an example of the chl a distribution in an Arctic multi-year ice #oe collected at station 218 in the East Greenland Current in August 1994. Low-bulk salinities and relatively high temperatures are typical for Arctic summer sea ice. The calculated brine volume varied between 10 and 30% of the total ice volume. The Chl a pro"le clearly showed a well-developed bottom community with concentrations above 50 mg chl a m\ ice in the lowermost centimetres. The actual Chl a concentration within the brine channel system was far higher, exceeding 400 mg chl a m\ brine (Fig. 2). Ice temperatures (Fig. 3a) ranged between !1.6 and 0.93C in the Arctic summer. In autumn, ice was colder with values of !6.4}0.13C. The seasonal variation of the ice bulk salinity (Fig. 3b) was very small from 0.0 to 7.0 in summer to 0.0}9.2 in autumn. The relative brine volume (Fig. 3c) was lower in autumn 1995 than in summer 1994 due to lower temperature and salinity. The chlorophyll a concentrations (Fig. 4) in the brine were higher in autumn than in the summer with a maximum value of 2210 mg chl a m\ brine in the bottom 2 cm of one ice #oe. The integrated chlorophyll a concentrations (Fig. 5) ranged between 0.1 and 3.3 mg chl a m\ with a slightly, but not signi"cantly (p"0.1; Mann}Whitney U-Test) higher median of 2.0 mg chl a m\ in the autumn than in the summer (median of 1.2 mg chl a m\).
Fig. 2. Temperature, salinity, brine volume and algal biomass in an ice core from station 218.
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Fig. 3. Data range of observed (a) ice temperature, (b) salinity and (c) calculated brine volumes for all pack ice samples during ARK X/1 (n"258) and ARK XI/2 (n"195). In the box plots the total data range and the 25}75% quartile range are shown. Single data points were marked as outliers, when they exceeded a value < of <"UQ#1.5 ) IQD or <"LQ!1.7 ) IQD (LQ"lower quartile, UQ"upper quartile, IQD"interquartile distance).
The major primary producers inside the sea ice were pennate diatoms, but we also observed considerable concentrations of #agellates (e.g., Fig. 6). Ciliates and metazoans were closely related to the vertical distribution of the algae with their highest concentrations in the lowermost 2 cm, although metazoans also occurred more than 1 m above the bottom of the ice #oes. On average (means), the sympagic summer
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Fig. 4. Calculated algal biomass in the brine of all ice samples during ARK X/1 (n"258) and ARK XI/2 (n"195). For explanation of box plots see Fig. 3.
community (integrated over entire ice thickness) consisted of 20.5;10 bacteria, 683;10 pennate diatoms, 65;10 centric diatoms, 799;10 phototrophic and 882;10 heterotrophic #agellates m\ ice. Sea-ice meiofauna mainly consisted of ciliates (83.6;10 m\), nematodes (21.6;10 m\), acoel turbellarians (5.5;10 m\), copepods (2.4;10 m\), and rotifers (2.2;10 m\). Based on the microscopical analyses of the ice cores, we calculated the organic carbon concentration within the sea ice of the Greenland Sea (Fig. 7). Integrated mean biomass of all sea ice organisms added up to 195.6 mg C m\ sea ice. Bacteria contributed the largest fraction of organic carbon (31%) followed by pennate diatoms (26%), heterotrophic (20%) and phototrophic (17%) #agellates. The meiofauna contributed only a minor fraction to total biomass (3.7%). Nematodes (1.5%), acoel turbellarians (0.9%) and copepods (0.8%) were the dominant metazoa in the ice cores. The mean ratio of heterotrophic to phototrophic biomass was 2.0. Relative to the phototrophic biomass, which was set to 1, bacterial biomass was 1.2$0.5 (standard error), for protozoa 0.6$0.1 and for meiofauna 0.2$0.1.
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Fig. 5. Integrated algal biomass in pack ice from the Greenland Sea (this study), the central Arctic Ocean (Gradinger, unpubl. data) and three fast ice regions (Cota et al., 1991; maximum levels were provided). For explanation of box plots see Fig. 3. Horizontal lines inside the boxes of the pack ice data indicate median values.
Fig. 6. Biomass of bacteria, pennate diatoms, photo- and heterotrophic protists and abundance of sea ice meiofauna in an ice core from station 216.
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Fig. 7. Integrated biomass of the sea-ice biota (n"6 ice cores) in the Greenland Sea in summer 1994. For explanation of box plots see Fig. 3. Horizontal lines inside the boxes indicate median values.
Martin and Wadhams (1996) provided the annual ice #ux rates for the Greenland Sea in 1994. Their data showed that 530;10 m sea ice melt between 793N and 703N. This melt leads to a release of sympagic biomass of roughly 0.104 Tg C y\, if we assume a biomass of the sympagic community of 0.2 g C m\ ice (Fig. 7). Most of the ice melt (71%) takes place between 763N and 753N, which leads to an input of about 0.074 Tg C y\ from the ice into the pelagic realm in this area. The carbon-based grazing model of Moloney and Field (1989) allowed us to estimate the potential grazing impact of sea ice meiofauna (Fig. 8). The calculated weight speci"c ingestion rates ranged between 1.44 d\ (ciliates) and 0.52 d\ (copepods) at a temperature of !13C. The total meiofauna community had a potential daily ingestion rate between 2.1 and 11.2 mg C m\ d\ with an average of 5.5 mg C m\ d\ at the investigated stations. For further calculations, we assumed that this activity only occurs during the Arctic productive summer phase (120 days) leading to a total potential ingestion of 656 mg C m\ (120 d)\.
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Fig. 8. Potential maximum ingestion rates of sea-ice meiofauna (n"6 ice cores) in the Greenland Sea in summer 1994. For explanation of box plots see Fig. 3. Horizontal lines inside the boxes indicate median values.
4. Discussion Major regions of ice formation are located on the Russian shelf areas, i.e., the Kara Sea, Laptev Sea and East Siberian Sea (Carmack and Swift, 1990). From these areas, the ice #oes are transported by the Transpolar Drift through the central Arctic Ocean until they enter the Greenland Sea through the Fram Strait and subsequently melt. About 10% of the sea ice in the Arctic basin is exported each year through Fram Strait into the Greenland Sea (Maykut, 1985). Hence, our sampling took place in the major export area of multi-year drift ice from the central Arctic. Our results may be representative for the ice conditions within the Arctic basin; the integrated algal biomass data from ARK X/1 and ARK XI/2 "t into the data range obtained during the Polarstern summer expedition ARK VIII/3 in the central Arctic (for cruise details see FuK tterer, 1991), where we sampled 47 ice #oes up to 903N (Fig. 5; Gradinger, unpubl. data). Published data from coastal fast ice areas (Cota et al., 1991) are orders of magnitude higher, indicating di!erent growth conditions for algae in di!erent types of sea ice. The lower biomass in drifting pack ice can be attributed to lower nutrient supply, di!erent physical parameters (ice temperature, brine salinity, radiation) or biological interactions (grazing and growth rates). Nitrate concentrations in ice cores during ARK X/1 were below the detection limit in most parts of the ice ((0.1 mmol m\; Gradinger unpubl. data) and only slightly higher close to the bottom of the ice #oes. Thus, limited nitrogen resources in ice #oes may limit algal development in the #oe interiors, such as in the coastal sea ice of the Canadian Arctic (Cota et al., 1987; Demers et al., 1989). Therefore, the exchange of dissolved inorganic nutrients between sea-ice brine channels and the pelagic realm in#uences the ice algal primary production (Cota et al., 1987; Gradinger et al., 1992). Besides nutrient supply,
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the marked seasonal variation of environmental factors a!ects the distribution and total biomass accumulation of ice organisms. Arctic ice diatoms are, however, euryhaline and can grow over a wide range of salinities (Grant and Horner, 1976; Zhang et al., in press), Antarctic ice diatoms even at salinities of 95 and !5.53C temperature (Bartsch, 1989). Antarctic and Arctic sympagic copepods have much higher salinity tolerances than pelagic ones (Dahms et al., 1990; Grainger and Mohammed, 1990). Our studies (Friedrich, 1997) and that by Grainger and Mohammed (1990) show that Arctic sea-ice metazoans are euryhaline and not restricted in their distribution inside the ice by temperature or brine salinity during the Arctic summer. They even occur more than 1 m above the underside of the ice #oes (e.g., Fig. 6). However, winter conditions with ice temperatures below !103C and brine salinities above 140 are lethal at least for acoel turbellarians and copepods (Friedrich 1997). Thus, winter survival probably causes, to a large extent, the distribution patterns that are typical for the Arctic bottom-ice communities we observed in summer and autumn. To validate this hypothesis, sea-ice data from early spring and the winter period are needed. The traditional view of the sympagic algal community, summarised by Poulin (1990), has diatoms as the main primary producers in Arctic sea ice. Our study is the "rst that attempts to evaluate the contribution of small #agellated taxa to total ice algal biomass, based on the analysis of entire sea ice cores. The #agellates contribute signi"cantly to overall biodiversity (IkaK valko and Gradinger, 1997). Phototrophic protists other than diatoms provided an average of 40% to the entire algal biomass and were even dominant in some cores. Autecological studies on sea-ice algae have been conducted only with sympagic diatoms from the Arctic and Antarctic (e.g., Bartsch, 1989; Gleitz et al., 1996), and it is questionable if these results can be extrapolated to #agellates. The high abundance of heterotrophic #agellates further increases the diversity of the sympagic community and indicates a microbial food web inside the ice, as already proposed by Laurion et al. (1995). The ice meiofauna composition was similar to that in early spring (Gradinger et al., 1991), with nematodes, acoel turbellarians and ciliates as most abundant taxa. Meroplanktic larvae of benthic polychaetes and molluscs, which inhabit coastal fast ice (Carey and Montagna, 1982), were never observed in any of the ice cores of the Greenland Sea. The overall composition of the sympagic community was very similar to results from oceanic pelagic habitats, where the ratio of heterotrophic (bacteria#protozoa# metazoa) to phototrophic biomass is close to 1.9 (Gasol et al., 1997). Consequently, also in Arctic sea ice we found an `inverted trophic pyramida. Gasol et al. (1997) proposed that such communities develop due to high algal biomass-speci"c activities. In the case of ice algae, typical P ratios are below 0.4 mg C mg C\ d\ (Cota and Smith, 1991), which is close to values obtained for coastal phytoplankton populations. Consequently, we assume that algal growth parameters alone cannot be responsible for the observed trophic pyramid in the sea ice. Further factors in#uence the trophic structure of the sea ice food web. The delicate structure of the brine channels leads, for example, to a spatial exclusion of larger predators as can be seen from their relatively low contribution to overall biomass compared to pelagic data from both oceanic and coastal locations.
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Present knowledge on grazing as a structuring factor for the development of sea-ice biota is still very poor and basic. Laurion et al. (1995) gave "rst estimates on grazing rates of heterotrophic protists on ice bacteria, which are similar to rates in other marine aquatic habitats. To date, no estimate exists for the impact of the sea-ice meiofauna. Our grazing model suggests, as a rough estimate, a potential carbon ingestion by meiofauna of about 650 mg C m\ during the productive Arctic summer (120 days). Legendre et al. (1992) proposed an annual primary production by Arctic multi-year sea-ice algae of about 600 mg C m\. Thus, the carbon ingestion by meiofauna is on the same order of magnitude as the primary production. It follows that, in addition to limited nutrient supply, grazing by sea-ice meiofauna may control the accumulation of organic biomass in the sea ice. This result is in contrast to that of, e.g., Meguro et al. (1967), who suggested that there was no grazing in the ice. Estimates on the role of ice metazoa from coastal areas are not available. We noticed the ingestion of diatoms by the acoel turbellarians as did Grainger and Hsiao (1990), but we did not observe any food uptake by nematodes. The available food concentration inside the brine channels is 1}5 orders of magnitude higher than typical algal biomass in the water column of ice-covered Arctic waters or in marginal ice zone blooms (Gradinger and Baumann, 1991). Grazing might thus be prolonged into the dark season so that the annual grazing rate is higher than our estimate for 120 days. Furthermore, we did not include protists other than ciliates in our calculations because we assumed that they are primarily bacterivorous. However, some species such as heterotrophic euglenophytes or dino#agellates are known to feed on pennate diatoms (Buck et al., 1990; IkaK valko and Gradinger, 1997), leading to even higher potential ingestion. The discrepancy between previous primary production estimates for Arctic multi-year ice #oes (Legendre et al., 1992) and our calculations of potential grazing e!ects, as well as in-situ algal biomass both for the inside of the sea ice and the top of the #oes (Gradinger and NuK rnberg, 1996), present further evidence to the statement of Wheeler et al. (1996) that primary production within the icecovered Arctic Ocean is at least one order of magnitude greater than previously assumed. The Greenland Sea is the major melting area for sea ice leaving the central Arctic Ocean by the Transpolar Drift. Thus, the entire ice biota is released into the water column there and may either contribute to pelagic production or sink to the sea #oor. We estimated an annual release of organic biomass of about 0.1 Tg C y\ from melting ice into the water column between 79 and 703N for 1994. Compared with the annual new production by phytoplankton (56 g C m\ y\; Noji et al., 1996), the input of carbon from the ice to the water column is of minor importance for the organic carbon cycle of the Greenland Sea. Nevertheless, the release may have considerable in#uence on the pelagic and benthic realms. The released algae may either initiate the spring algal plankton bloom (Smith and Sakshaug, 1990) or they may sink to the sea #oor and serve as an episodic and "rst food pulse for benthic organisms before pelagic production begins (Carey, 1987). Future models on the carbon budget of ice covered areas such as that by Slagstad et al. (1996) should therefore include a coupled ice-pelagic component.
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Acknowledgements The helpfulness of the crew of the RV Polarstern is gratefully acknowledged. We would like to thank our colleagues for assistance during the expeditions and fruitful discussions at sea and in the home labs. This study was supported by the Commission of the European Community under contract MAS2-CT93-0057 of the MAST-II programme. The Deutsche Forschungsgemeinschaft (DFG Gr 1405/1-1) provided the microscopical equipment used by RG.
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