Spatial and Temporal Variations in Deep-Sea Meiofauna Assemblages in the Marginal Ice Zone of the Arctic Ocean

ARTICLE IN PRESS

Deep-Sea Research I 54 (2007) 109–129 www.elsevier.com/locate/dsr

Spatial and temporal variations in deep-sea meiofauna assemblages in the Marginal Ice Zone of the Arctic Ocean

Eveline Hostea,Ã, Sandra Vanhovea, Ingo Scheweb, Thomas Soltwedelb, Ann Vanreusela

aMarine Biology Section, University of Gent, Krijgslaan 281-S8, B-9000 Gent, Belgium bAlfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany

Received 12 January 2006; received in revised form 13 September 2006; accepted 19 September 2006 Available online 16 November 2006

Abstract

In order to understand the response of the deep-sea meiobenthos to a highly varying, ice-edge-related input of phytodetritus, we investigated the abundance and composition of the meiobenthos at the arctic long-term deep-sea station HAUSGARTEN (791N, 41E) along a bathymetric transect (1200–5500 m water depth) over 5 consecutive years (from 2000 to 2004) in relation to changes in environmental conditions. Results showed high sediment-bound pigment concentrations (chlorophyll a and degradation products) ranging from 4.5 to 41.6 mg/cm3, and coinciding high meiobenthic densities ranging from 14973to 34097525 ind/10 cm2. Nematodes dominated the metazoan meiofaunal communities at every depth and time (85–99% of total meiofauna abundance), followed by harpacticoid copepods (0–4.6% of total meiofauna abundance). The expected pattern of gradually decreasing meiobenthic densities with increasing water depth was not conﬁrmed. Instead, the bathymetric transect could be subdivided into a shallow area with equally high nematode and copepod densities from 1000 to 2000 m water depth (means: 22597157 Nematoda/10 cm2,and5074 Copepoda/10 cm2), and a deeper area from 3000 to 5500 m water depth with similar low nematode and copepod densities (means: 595752 Nematoda/10 cm2,and1172 Copepoda/10 cm2). Depth-related investigations on the meiobenthos at the HAUSGARTEN site showed a signiﬁcant correlation between meiobenthos densities, microbial exo-enzymatic activity (esterase turnover) and phytodetrital food availability (chlorophyll a and phaeophytines). In time-series investigations, our data showed inter-annual variations in meiofauna abundance. However, no consistent relationship between nematode and copepod densities, and measures for organic matter input were found. r 2006 Elsevier Ltd. All rights reserved.

Keywords: Arctic; Greenland Sea; Deep water; Benthos; Meiofauna; Abundances

1. Introduction however, are some of the most dynamic areas in the world’s oceans with large seasonal, inter-annual and Polar oceans are extreme environments with low spatial ﬂuctuations in ice-cover and high ice-related temperature and seasonal light and food limitation, primary production (Falk-Petersen et al., 2000). which exert major inﬂuences on global climate and This variability is a critical factor, which structures ocean systems. The Marginal Ice Zones (MIZs), the arctic marine ecosystem. The spring phytoplankton bloom follows the ÃCorresponding author. Tel.: +32 09264 85 23. receding ice edge as it melts (Sakshaug and Skjoldal, E-mail address: [email protected] (E. Hoste). 1989) and intensive blooms occur in leads as the

MIZ opens up (Schewe and Soltwedel, 2003). The environmental variables on meiobenthos densities development of such blooms requires 2–3 weeks of in time and with water depth. open water, a relatively stable ice cover during This study addresses the following questions. Are winter, and stratification of the water column deep-sea meiofauna densities along the productive (Falk-Petersen et al., 2000; Engelsen et al., 2002). MIZ higher than in other polar deep-sea regions? One to 2 months prior to the pelagic production, ice Do meiofauna densities and vertical depth profiles algal production is initiated (Falk-Petersen et al., in the sediment change along a bathymetric 2000). In ice-free areas of the MIZ to the north- transect? Do meiofauna densities and vertical depth west of Svalbard, primary production rates of profiles change over time? Are these changes 18–20 mg cm2 h1 were measured, while at the correlated with organic matter input or other ice-edge, production rates even increased up to environmental variables? Are influences of time- 37 mg cm2 h1 (Heimdal, 1983). related changes in environmental variables on Several studies in the deep sea indicated a rapid meiofauna densities comparable to influences of downward transport of fresh phytodetritus and depth-related changes in environmental variables? fecal pellets (Billett et al., 1983; Graf, 1989) and The goal of this study was to gain a better possibly a rapid processing of this material by the understanding of the relation between benthos and deep-sea benthos, which is sustained by this organic environmental variables possibly related to ice matter from the euphotic zone (Moodley et al., conditions. 2002; Witte et al., 2003). The flux of organic matter to the deep seafloor, however, is highly variable in 2. Material and methods time and space. At high latitudes, inter-annual variations in ice coverage determine the start and 2.1. Sampling site intensity of the phytoplankton bloom (Sakshaug and Skjoldal, 1989). As the presence and persistence The long-term deep-sea observatory HAUS- of life at the ocean floor can be seen as a response to GARTEN is situated in Fram Strait, west of organic matter input (Thiel, 1975; Gooday and Svalbard at 79 1N(Soltwedel et al., 2005). The Turley, 1990; Grebmeier and Barry, 1991; Gooday, majority of the sampling sites in this area form a 2002), the variability in organic matter fluxes to the bathymetric transect of nine stations from the upper seafloor is bound to have an influence on the slope of the Svalbard Margin (1200 m) to Molloy benthos. Hole (75500 m), the deepest depression recorded in To investigate the impact of large-scale environ- the Arctic Ocean (Myhre and Thiede, 1995)(Fig. 1). mental changes in the transition zone between the The sampling sites between 1200 and 2500 m water North Atlantic and the central Arctic Ocean, and to depth are located on a gentle slope while stations determine the factors controlling deep-sea biodiver- between 3000 and 5000 m are located on a steep sity, the German Alfred Wegener Institute for Polar slope (up to 401 inclination between 4000 and and Marine Research (AWI) established the deep- 5000 m) towards Molloy Hole (Fig. 1)(Soltwedel sea, long-term observatory HAUSGARTEN, re- et al., 2005). presenting the first, and by now only, open-ocean, Hydrographic conditions in the HAUSGARTEN long-term station in a polar region (Soltwedel et al., area are characterized by the inflow of relatively 2005). In this part of the HAUSGARTEN research warm and nutrient-rich Atlantic Water into the project, the emphasis is on the impact of changing central Arctic Ocean (Manley, 1995). Circulation environmental variables on the metazoan meio- patterns in the Fram Strait result in a variable sea- benthos. ice cover, with permanent ice-covered areas in the Food quality and quantity reaching the deep- west, permanent ice-free areas in the southeast, and seafloor decreases with increasing water depth seasonally varying conditions in central and north- (Billett et al., 1983; Falk-Petersen et al., 2000; eastern parts, where the HAUSGARTEN area is Engelsen et al., 2002; Schewe and Soltwedel, 2003). located (Soltwedel et al., 2005). As food availability is thought to be the most important structuring factor for meiobenthos com- 2.2. Sampling strategy munities, the unique combination of a time series along a bathymetric transect at the summer MIZ Samples were obtained during cruises ARK-XVI allows us to analyze the impact of changing to ARK-XX of the German ice-breaker R.V. ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 111

Fig. 1. Map of the Greenland Sea with Sea minimum (2004) and maximum (2003). Ice concentration in Juli (http://nsidc.org/sotc/ sea_ice.html), a detail of the sampling transect and detail of the bathymetric transect.

Polarstern, in the summer months of 2000–04. A Bengal, counted and identified up to higher taxon multiple-corer (MUC) was used to collect sediment level. For technical and logistical reasons, meiofau- cores with virtually undisturbed surfaces (Gage and na samples are missing for 2000, 5000 and 5500 in Tyler, 1991). For meiofaunal analysis, 3 samples 2001, for 5500 m in 2000 and 2002, and for 5000 m from different cores of the same MUC haul were in the years 2003 and 2004. taken by means of a modified plastic syringe Samples for biogenic sediment compounds (in- (3.14 cm2 cross-sectional area) and subdivided into dicators for organic matter input, sediment-bound 1 cm slices down to 5 cm sediment depth in order to biomass and microbial activity) were also taken study the vertical distribution of the meiofauna in with modified syringes (1.17 and 3.14 cm2 cross- the sediment. After elutriation with the Ludox sectional area) and analyzed at 1-cm-intervals down centrifugation method (Heip et al., 1985) all to 5 cm sediment depth. Sediment composition, metazoan organisms passing a 1 mm sieve and determined using a Coulter Counter LS 100TM, retained on a 32 mm sieve were stained with Rose was only analyzed for the 2001 samples, and are ARTICLE IN PRESS 112 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 lacking for 2000 and 5000 m water depth. Also, in All statistical analyses were performed on the 2001, data on organic matter input are lacking for original meiofauna densities per 3.6 cm2. Formal the station at 4000 m water depth. significance tests for differences in taxon community Concentrations of chloroplastic pigments (chlor- structure between the depths and years were carried ophyll a [Chl a] and its degradation products ¼ out using the one-way ANOSIM tests (Clarke, chloroplasic pigment equivalents [CPE]; Thiel, 1993), performed on the Bray–Curtis similarity 1978) in sediments were studied to estimate the indices. The square root transformed meiobenthos food availability, originating from plant material, at densities data were analyzed by non-metric multi- the deep seafloor. Chloroplastic pigments were dimensional scaling (MDS) using the Bray–Curtis extracted in 90% acetone and measured with a similarity measure. The relation between the meio- Turner fluorometer according to Yentsch and benthos and environmental variables was analyzed Menzel (1963) and Holm-Hansen et al. (1965). using the Spearman rank correlation (s) and the The percentage contribution of Chl a to the total significance was determined using a permutation pigment content (%Chl a) is used to indicate the procedure (RELATE; Clarke and Warwick, 1994). ‘freshness’ of the phytodetrital matter in the The BIO-ENV procedure (Clarke and Warwick, sediments. 1994) was used to define the environmental vari- Parameters related to organism biomass firstly ables that best determine the meiobenthos assem- include Ash-free Dry Weight (AFDW; estimation of blage structures. Finally, a Draftsman plot analysis total organic content) determined after combusting was performed to analyze further correlations sediment samples for 2 h at 500 1C. Secondly, between densities and environmental variables phospholipids (PL, indicating the total microbial resulting in Pearson correlation coefficients. For biomass) were determined by the method of Findlay the pairwise ANOSIM tests, R-levels were used et al. (1989) which involved conversion of the instead of p-levels because the number of permuta- phospholipid fatty acids to fatty acid methyl ester tions was possibly insufficient due to the small by treatment with 0.2 N KOH in methanol and number of samples within the compared groups. analyses by gas chromatography. Finally, particu- The following R-levels and correlation coefficient- late proteins (PP, indicating the biomass of small levels were used:40.75, well separated (ANOSIM) organisms and detrital matter) were analyzed or highly correlated (Draftsman plot); 40.5, over- photometrically following instructions given by lapping but clearly separated or well correlated and Greiser and Faubel (1988). As esterases are involved o0.25, barely separable at all (Clarke and Gorley, in primary decomposition of organic matter, the 2001) or not correlated at all. For all other analyses potential activity of such enzymes was measured a significance level of po0.05 was used. All analyses using the fluorogenic substrate Fluorecein-di-acet- were performed using the PRIMER v5.2.9 software ate (FDA), according to the method described by package (Clarke and Gorley, 2001). Ko¨ ster et al. (1991). 3. Results 2.3. Data analyses 3.1. Environmental variables The environmental variables along the depth transect and over the time series were analyzed Silt (2–63 mm) was the dominant grain size using a correlation-based principal component fraction over the bathymetric gradient, ranging analysis (PCA). Prior to the PCA the environmental from 43% (2500 m) to 55% (1000 m). The 5500 m data were analyzed using a Draftsman plot (Pearson station had the finest sediment and the 2500–4000 m correlation coefficients; Clarke and Warwick, 1994) stations had the coarsest sediment (Fig. 2). in order to detect correlations between environ- In general, sediment-bound chloroplastic pig- mental variables and to verify the need for ments (Chl a, 0–5 cm) decreased with water depth transformation. Since CPE values were correlated till 4000 m and increased again at greater depths with Chl a and phaeopigments, they were excluded (Fig. 3(A)–(C); Table 1). Although the highest from the analysis and other environmental data values were found at the shallowest stations, Chl were square-root transformed except for depth and a, phaeophytines and %Chl a were not correlated %Chl a, which were log(x+1) transformed (Clarke with water depth (Table. 2). Also, not all indicators and Warwick, 1994). for biomass (Fig. 4(A)–(C); Table 1) were correlated ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 113

clay (<2µm) silt (2µm-63µm) sand (63-2000 µm) with water depth. Only FDA (0–5 cm) decreased 100% (signiﬁcantly, R ¼0.587, N ¼ 38, Table. 4) with 90% water depth along the bathymetric gradient (Fig. 5, Table 1). Highest AFDW and PL (0–5 cm) values 80% were recorded in the year 2000 at most stations. 70% Exceptions were the maximum values of AFDW 60% (0.789 mg/cm2) at 1500 m (recorded in 2004) and of 50% PL at 4000 m (2001, 2002). PP showed a completely 40% different pattern with highest values found in 2004 at all the stations, with the exception of the 2000 m 30% station. 20% Axis 1 of the PCA plot (Fig. 6), including all 10% environmental variables except sediment grain size 0% fractions, explained 41.2% of the variation in the 1200 1500 2500 3000 3500 4000 5500 data, while axis 2 explained only 20.2%. The primer depth (m) analysis gives water depth, indicators for food input Fig. 2. Grain size fractions over the bathymetric depth for 2001. (Chl a and phaeopigments) and FDA as the primary

45 1.2 2000 2000 2001 40 2001 2002 2002 1.0 2003 2003 35 2004 2004 ) 2 30

) 0.8 2 g/cm µ 25 g/cm µ 0.6 20 Chl a ( 0.4 15 phaeopigments ( 10 0.2 5

0.0 0 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 (A)depth (m) (B) depth (m)

3.5

2000 3.0 2001 2002 2003 2004 2.5

2.0

%-Chl a 1.5

1.0

0.5

0.0 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 (C) depth (m)

Fig. 3. Pigment data (0–5 cm) over the 5-year time series. (A) chlorophyl a (Chl a), (B) phaeopigmnents (Phaeo) and (C) percentile Chl a over total organic content (%Chl a). ARTICLE IN PRESS 114 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 ) 2 SE (ind/10 cm ) 2 MEIO (ind/10 cm ) 1 h 1 FDA (nmol ml ) 3 PL (nmol cm ) 3 gcm m PP ( ) 3 gcm m AFDW ( a (%) ) %Chl 3 gcm m CPE ( ) 3 gcm m Phaeo ( ) 3 a gcm m Chl ( , Phaeo: phaeopigmentsand, CPE: chloroplasic pigment equivalents), biomass data (AFDW: ash-free dry weight, PP: particulate a Water depth (m) 12461495 1.161929 0.632385 0.462802 36.02 0.213350 29.08 0.154020 26.61 0.08 37.185079 18.19 0.11 29.711284 13.03 0.25 27.071524 0.62 9.76 18.402468 12.52 0.22 13.172916 24.29 0.13 3.003348 34.37 0.07 1.71 9.84 12.633997 20.10 0.06 0.69 1.56 24.541292 15.74 — 0.71 1.12 34.981559 12.26 0.57 0.72 1.02 20.321928 10.71 2.30 0.30 0.71 15.872469 0.70 2.20 0.65 0.74 0.82 12.332899 — 29.29 2.36 0.11 0.93 10.773640 0.76 118.23 16.91 1.61 0.20 0.61 1.594039 149.27 23.06 1.22 0.20 0.66 1.05 29.875231 115.71 13.01 — 0.09 0.65 0.78 17.201277 1.18 11.08 15.49 1.18 0.03 0.60 0.49 73.87 23.721551 172.77 1.72 0.58 0.59 0.36 6.52 8.39 13.121912 11.81 1.95 0.36 0.64 5.60 15.702501 148.76 2.15 0.10 0.57 1.82 56.01 4.973129 6.68 41.01 1.72 0.23 1.38 8.59 47.91 2.79 — 2604 11.903491 30.37 1.36 0.00 0.59 2.69 52.424097 1993 1.24 1.84 0.10 0.60 0.75 5.00 81.51 5.37 41.595573 1.55 2399 28.93 0.05 0.64 1.17 60.94 0.62 30.731280 2.84 17.09 2.59 722 0.17 0.57 92.79 31.671554 569 1227 1.39 15.18 2.53 0.38 0.61 0.51 5.47 73.58 20.17 29.162050 84 22.53 3.11 0.23 1.22 237 17.092507 8.90 0.52 0.17 28.60 2.00 426 0.15 0.51 1.27 11.76 46.41 15.283136 568 20.44 2.06 0.17 1.04 72.01 183 22.583574 30 747 6.10 3249 100.35 0.52 14.97 0.15 0.55 79.09 28.764089 1.29 1768 1.75 10.59 2.53 0.25 0.51 0.62 27.19 35.87 20.825570 58 10.64 0.05 208 0.00 1824 28.39 27.81 15.21 1.49 0.52 27.13 2.94 0.22 0.50 244 0.56 672 9.84 10.75 22 2.53 12.86 2.67 39.39 0.53 0.10 15.85 81.07 216 10.81 561 0.51 0.45 4.43 8.39 2.73 310 2656 11.55 2.23 31.33 0.46 1.84 9.99 73.21 13.11 2410 1.59 0.42 76 1.54 58.14 4.12 3409 6.32 1.62 0.50 1.44 4.48 11.77 34 810 2059 1.82 30.69 0.79 1.59 47.52 43.67 133 1.76 2.42 0.49 58.93 114 725 4.66 1.52 3.61 526 0.53 1.93 62.07 3.26 25.72 17.03 57.58 163 135 501 668 0.48 1.13 1.76 0.48 1.83 24.86 4.90 2525 2.82 52.65 340 53 6.46 0.46 0.47 1805 15.79 4.11 2.25 1.60 168 52.47 76 2139 4.21 1616 21.47 238 6.29 3.09 2.76 25 605 3.75 25.46 79 25.81 674 7.56 325 86 407 2.37 13.84 21.72 841 3303 4.83 75 2.44 171 1658 1540 1.15 58 1.66 122 888 78 31 765 452 163 150 45 888 109 91 74 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 06,19 53.60 36.20 11.20 43.40 36.00 28.80 21,36 04.50 54.40 10.40 42.80 36.20 29.20 05.49 53.91 36.40 10.93 43.45 32.40 28.87 19.63 05.54 54.04 36.38 07.57 39.43 34.54 28.49 50.73 05.46 54.07 50.25 04.98 39.25 33.78 28.57 50.64 : chlorophyll 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 a E Longitude 1 06 04 04 04 03 03 03 03 06 04 04 03 03 03 06 04 04 04 03 03 03 03 06 04 04 04 03 03 03 02 06 04 04 04 03 03 03 02 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 07.80 06.50 04.10 03.86 04.50 03.60 04.48 08.00 08.10 04.00 04.10 05.30 04.00 08.44 07.84 06.51 03.90 03.99 05.10 03.60 04.52 08.00 07.80 06.50 04.31 03.78 03.53 03.57 07.99 07.99 07.76 04.02 05.00 03.78 03.82 03.56 08.02 08.28 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 N PositionLatitude 1 Organic matter input Biomass Activity Densities Sampling date Table 1 Station data (0–5 cm) from sampling sites alongStation the Hausgarten bathymetricNo. gradient sorted by sampling year and water depth Values for organic matter input (Chl proteins, PL: phospholipids), activity (ﬂuorescein–diacetate) and mean meiofauna densities with the standard error (SE) are given. PS57/166–2PS57/168–2 03/08/2000PS57/178 03/08/2000 79 PS57/176–2 79 05/08/2000PS57/181 04/08/2000 79 PS57/182–2 79 05/08/2000PS57/252 06/08/2000 79 PS59/91 79 17/08/2000PS59/96 79 PS59/94 12/07/2001PS59/103 14/07/2001 79 PS59/105 13/07/2001 79 14/07/2001PS59/108 79 15/07/2001 79 PS62/171–2 15/07/2001 79 PS62/170–2 06/08/2002 79 PS62/162–2 05/08/2002 79 PS62/161–2 03/08/2002 79 PS62/169–2 02/08/2002 79 PS62/163–2 05/08/2002 79 PS62/183–2 03/08/2002 79 PS62/185–3 08/08/2002 79 PS64/402 09/08/2002 79 PS64/408 79 21/07/2003PS64/439 21/07/2003 79 PS64/429 26/07/2003 79 PS64/414 26/07/2003 79 PS64/419 23/07/2003 79 PS64/464 24/07/2003 79 PS64/471 02/08/2003 79 PS66/104–1 03/08/2003 79 PS66/101–2 07/07/2004 79 PS66/100–2 07/07/2004 79 PS66/117–1 07/07/2004 79 PS66/114–2 09/07/2004 79 PS66/121–2 09/07/2004 79 PS66/122–2 10/07/2004 79 PS66/124–2 10/07/2004 79 11/07/2004 79 79 PS57/272 19/08/2000 79 ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 115

Table 2 Pearson correlation matrix with the variables water depth (depth), chlorophyl a (Chl a), phaeopigments (Phaeo), chloroplastic pigment equivalents (CPE), ash free dry weight (AFDW), particulate proteins (PP), phospolipids (PL), bacterial esterase activity (FDA), meiobenthos density (MEIO), nematode density (NEMA) and copepod density (COP)

Levels of correlation: black 40.75; grey 40.50; white o0.50. variables explaining the variation along the first Fig. 7 shows the mean nematode and copepod axis. Two groups could be observed: (1) from 1000 densities along the bathymetric transect over the to 2000 m water depth and (2) from 2500 to 5000 m 5-year period. Mean densities (0–5 cm) ranged water depth (Fig. 6(A). The second PC axis was between 13576 nematodes/10 cm2 (4000 m, in primarily determined by the indicators for biomass 2004) and 32157497 nematodes/10 cm2 (2000 m; (PP, AFDW, and PL). No clear separation between in 2002). Harpacticoid copepod densities ranged the years could be observed but there was a gradual from 171ind/10cm2 (2500 m, in 2000) to 80713 ind/ transition in time along the axis due to a general 10 cm2 (2000 m, in 2002). decrease in AFDW and PL in time (Fig. 6(B)). Both nematode and copepod densities were correlated with water depth (R ¼0.766 [N ¼ 8] and R ¼0.661 [N ¼ 38], respectively) per year and 3.2. Meiobenthos communities over all years. The correlation between densities and depth, however, does not reflect a linear relationship In total, 40,311 metazoan meiobenthos organisms but is rather due to the high difference in densities were counted. These organisms belonged to 18 between a 1000–2500 m zone and a 3000–5000 m major taxa. Taxon richness ranged from 1 taxon zone. Nematode and copepod densities were (Nematoda), to over 10 taxa per station (Table 3). also correlated with phaeopigments, %Chl a, PP, Mean meiobenthos densities for each station over and FDA in individual years and over all years the time series are given in Table 1. Nematodes were (Table 2). However, no significant correlation with always the most abundant metazoan taxon Chl a was found. (85–99%), making up 95% of the total meiofauna The ANOSIM results indicated that the meio- at all dates and water depths. Harpacticoid cope- benthos communities were significantly different pods were the second most abundant taxon (0–4.6% between water depths (R ¼ 0.50, po0.001). Look- and 1.9% of the total meiofauna) and also nauplii ing at the pairwise tests between stations, differences were consistently present (0–4% and 1.6% of the occurred especially between the 1200–2000 m zone total meiofauna). Other taxa such as polychaetes, and the 3000–5500 m zone. The station at 2500 m gastrotrichs, kinorhynchs, tardigrades, rotifers and depth was significantly different from all other tantulocarids were regularly found but in very low stations. The overall meiobenthos community did abundances (max 2%). not differ over the years (R ¼ 0.032, p40.05) but ARTICLE IN PRESS 116 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129

0.85 4.0 2000 2000 0.80 2001 3.5 2001 2002 2002 2003 2003 0.75 2004 3.0 2004 ) ) 3

0.70 2 2.5 0.65 2.0 0.60 1.5 proteine (mg/cm

AFDW (mg/10cm 0.55 1.0 0.50

0.45 0.5

0.40 0.0 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 (A) depth (m) (B) depth (m)

180 2000 160 2001 2002 2003 140 2004

) 120 2

100

lipide (nmol/cm 60

0 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 (C) depth (m)

Fig. 4. Biomass data (0–5 cm) over the 5-year time series. (A) Ash-free dry weight (AFDW), (B) particulate proteins and (C) phospholipids. looking at each water depth separately there were The shallow group had high nematode and copepod significant differences between the years for the densities with a mean density of 22597157 ind/ stations between 2000 and 3000 m and the 4000 m 10 cm2 and almost 5074 ind/10 cm2, respectively, station. The pattern over time for these water whereas the deep group had a mean nematode depths, however, was different for each depth density of about 595752 ind/10 cm2 and a mean (Fig. 8). copepod density of 1172 ind/10 cm2. Only the The similarity matrix based on the Bray–Curtis station at 2500 m had an intermediate position; similarities of meiofauna densities were significantly depending on the year it grouped with one or both (Rho ¼ 0.401; p ¼ 0.001) related to the normalized of the depth-related groups. However, a temporal Euclidian distance similarity matrix of the environ- trend was not observed. The changes in biomass mental data. When the BIO_ENV procedure was (PP, AFDW, and PL) over time were thus not applied, water depth emerged as the environmental reflected in meiobenthos community structures. variable that best explained the variation in the Fig. 10 shows the vertical distribution of the meiobenthos data (Rho ¼ 0.570), as shown in the nematodes with sediment depth for the time series. MDS plot (Fig. 9). A low stress value (o0.2) for the The mean proportional nematode density in the first MDS analysis indicated a good ordination with no 2 cm of the sediment increased with depth real prospect of a misleading interpretation (Clarke, (R ¼ 0.922) along the transect, from a minimum 1993). The same shallow and deep groups of of 54% at 1000 m to 86% at 3500 m, and decreased stations appeared in the MDS plot as in the PCA. again to 60% at the 5500 m station. The mean ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 117

50 2000 45 2001 2002 2003 40 2004

20 FDA (nmol / ml h) 15

0 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 depth (m)

Fig. 5. Bacterial esterase activity (FDA) over 5 cm depth for the 5-year time series (%Chl a). proportional abundances in the first 2 cm were A significant decrease in Chl a and phaeopig- negatively correlated with nematode and copepod ments with increasing distance from the ice edge has densities (N ¼ 38, R ¼0.664 and 0.690, respec- been reported in several studies (Engelsen et al., tively) and FDA (N ¼ 38; R ¼ 0.506). Down to 2002; Schewe and Soltwedel, 2003). In ice–free areas 3500 m there was also a positive correlation with from the MIZ to the northwest of Svalbard, water depth (N ¼ 29; R ¼ 0.922). The inter-annual primary production rates of 18–20 mg cm2 h1 variability in sediment depth profile decreased with were measured, while at the ice-edge, production water depth along the bathymetric gradient. Varia- rates even increased up to 37 mg cm2 h1 (Heimdal, tions in the vertical distribution of nematodes were 1983). The POC input of 250 mg cm2 into the deep mainly observed at the shallowest stations (down to layers (200 m) at the Barents Sea MIZ could even be 2500 m). comparable to that in upwelling areas and is generally more than in coastal and shelf areas (Olli 4. Discussion et al., 2002). In this study, food availability at the seafloor was estimated by analyzing sediment- 4.1. Comparison of arctic MIZ meiobenthos and bound chloroplastic pigments (Chl a and Phaeopig- environmental parameters with other polar deep-sea ments), which showed, as expected, high values sites compared to most other polar deep-sea regions (Table 4). Similar high values were found along the Ice melting during the arctic spring and summer MIZ of the Fram Strait, near the HAUSGARTEN gives rise to a strongly stratified and nutrient-rich area (Schewe and Soltwedel, 2003), and on the euphotic zone, with a distinct phytoplankton Yermak Plateau (Soltwedel et al., 2000) where bloom. The phytoplankton bloom follows the lateral input under the ice, driven by the West receding ice edge as it melts during spring and Spitzbergen Current, causes comparably high Chl a summer (Sakshaug and Skjoldal, 1989) and inten- values in deep-sea sediments. As deep-sea benthic sive blooms occur in leads as the MIZ opens up. The ecosystems are sustained largely by the organic area of investigation, the HAUSGARTEN site, is matter settling from the euphotic zone (Beaulieu, situated along the summer MIZ in the Fram Strait 2002; Gooday, 2002), one might also expect high (Fig. 1) and sampling was performed in summer meiobenthos densities at HAUSGARTEN. Nema- when primary production and subsequent sedimen- tode and copepod densities were indeed high tation of organic matter was expected to be highest. compared to other deep-sea regions (Fig. 11), even ARTICLE IN PRESS 118 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129

3 1200m-2000m 2500m-5500m 1000 1500 2 2000 2500 1

0 3000 3500 PC2 -1 4000 5000

-2 5500 -3

-4 -5 -4 -3 -2 -1 0 1 2 3 4 (A) PC1

2000 2

1 2001

PC2 2002 -1

-2 2003

-3 2004 -4 -5 -4 -3 -2 -1 0 1 2 3 4 (B) PC1

Fig. 6. PCA plot including sediment bound pigments, biomass data and FDA with indication of (A) different depths and (B) different years. PC1 explains 41.2% of the variation; PC2, 20.2%. when differences in sampling technique (Table 4) due to the remineralization of organic matter during and processing are kept in mind. As in other deep- transport from the surface to the deep seafloor sea studies, nematodes clearly dominated the (Graf, 1989). There was, however, no significant metazoan meiofauna followed by copepods with correlation between depth and the chloroplastic other taxa such as Kinorhyncha, Tardigrada, and pigments along the studied transect because of the Gastrotricha present in very low numbers (Pfann- increase in food availability at 5000 and 5500 m. kuche and Thiel, 1987; Vanhove et al., 1995; These stations are located in the Molloy Hole, a Vanaverbeke et al., 1997; Schewe and Soltwedel, region that acts as a huge sediment trap accumulat- 1999; Vanreusel et al., 2000; Soltwedel et al., 2000; ing organic matter at the bottom (Soltwedel et al., Schewe, 2001). 2003). The increase in organic content of the sediment is reflected in the nematode and copepod 4.2. Bathymetric gradient densities, which are slightly higher in comparison with the other deep stations, illustrating the The decrease of meiobenthos densities with depth, importance of food input for meiobenthos densities. although stepwise and not gradually, is in accor- Contrary to most previous studies (Vanaverbeke dance with expectations based on the decreasing et al., 1997; Schewe and Soltwedel, 1999; Vanreusel quality and quantity of the food with water depth et al., 2000; see also review by Soltwedel, 2000), ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 119

Table 3 Meiofauna taxa (MEIO) and meiofauna densities (NEMA: nematodes, HARP: harpacticoid copepods, NAUPLII: nauplii and REST: bulk of all other taxaa) for each station in time

Station Water MEIO NEMA SE HARP SE NAUPLII SE REST* SE no. depth (# taxa) (ind/10 cm2) (ind/10 cm2) (ind/10 cm2) (ind/10 cm2) (m)

PS57/272 1246 6 2484 722 56 14 33 14 29 4 PS57/166–2 1495 6 1850 84 46 11 57 11 39 14 PS57/168–2 1929 7 2295 237 38 11 30 8 36 6 PS57/178 2385 3 557 30 1 1 5 2 9 4 PS57/176–2 2802 8 1172 183 14 1 7 3 37 10 PS57/181 3350 4 409 58 8 3 1 1 12 2 PS57/182–2 4020 5 535 208 8 3 10 3 21 4 PS57/252 5079 5 726 244 10 3 2 1 16 3 PS59/91 1284 7 3091 22 54 13 67 2 41 7 PS59/96 1524 8 1642 216 69 17 29 11 35 6 PS59/94 2468 7 1768 310 15 1 16 4 34 13 PS59/103 2916 7 618 76 14 3 8 5 44 10 PS59/105 3348 5 494 34 5 2 8 4 34 1 PS59/108 3997 5 783 163 6 0 8 7 26 2 PS62/171–2 1292 8 2514 133 47 6 63 1 46 11 PS62/170–2 1559 6 2282 114 54 5 51 15 37 3 PS62/162–2 1928 7 3211 526 80 13 82 26 51 5 PS62/161–2 2469 7 2014 135 17 8 10 2 35 4 PS62/169–2 2899 7 666 53 14 6 13 6 53 8 PS62/163–2 3640 5 474 76 7 1 3 2 38 5 PS62/183–2 4039 8 590 168 37 15 6 2 56 17 PS62/185–3 5231 4 316 25 12 9 4 4 31 3 PS64/402 1277 6 2390 238 61 17 50 19 44 7 PS64/408 1551 5 1690 79 45 2 47 12 47 4 PS64/439 1912 6 2028 86 42 6 38 2 55 10 PS64/429 2501 5 1562 325 17 4 17 5 45 9 PS64/414 3129 4 580 75 4 3 2 2 47 1 PS64/419 3491 5 647 171 11 1 8 1 37 3 PS64/464 4097 4 387 58 1 1 3 2 46 6 PS64/471 5573 4 796 122 27 3 12 3 38 1 PS66/104–1 1280 8 3110 78 52 6 90 15 80 3 PS66/101–2 1554 7 1564 31 32 5 37 6 58 4 PS66/100–2 2050 6 1481 163 23 5 12 2 59 6 PS66/117–1 2507 7 827 45 17 5 6 6 73 7 PS66/114–2 3136 5 714 91 10 2 5 3 73 5 PS66/121–2 3574 5 425 109 11 5 2 1 53 4 PS66/122–2 4089 2 135 4 1 1 0 0 54 4 PS66/124–2 5570 4 837 74 15 2 12 5 64 11

aOstracoda, Polychaeta, Rotifera, Gastrotricha, Kinorhyncha, Tardigrada, Isopoda, Bivalvia, Tantulocarida, Tanaidacea, Cumacea, Loricifera, Priapulida, Halacarida, Amphipoda, Sipunculida.

there was no gradual decrease in nematode and transect into two areas. The differences in topo- copepod densities with depth but rather a shallow graphy might inﬂuence near bottom currents, and deep area could be distinguished. The distinc- causing a sudden change in environmental condi- tion was also reﬂected in the environmental tions leading to a sudden drop in meiofauna variables and sediment characteristics. The topo- densities (Thistle and Levin, 1998). However, the graphy of the area, with the samples from 1200 to 2500 m station, although not located on the steep 2500 m located on a the gentle upper slope, and slope, groups with the steep slope stations based on samples from 3000 to 5000 m on the lower steep environmental data and shows a high inter-annual slope, might be the critical factor dividing the variability based on meiobenthos data. ARTICLE IN PRESS 120 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129

4000 2000 2001 3500 2002 2003 2004 2 3000

2500

2000

1500

nematode densities/10 cm 1000

500

0 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 (A) depth (m)

100 2000 2001 2002 80 2003 2004 2

40 copepod densities/10 cm 20

0 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 (B) depth (m)

Fig. 7. Mean nematode (A) and copepod (B) densities 7SE over the bathymetric transect for the 5-year time series.

The strong correlation of meiobenthos densities depths and the high predation pressure at Molloy with bacterial activity (FDA), for each year and Hole (Soltwedel et al., 2003) might also play a role. over all years, supports the assumed importance of To study the possible migration in the sediment bacteria as primary food source for the deep-sea with changing food availability (Vanreusel et al., metazoan meiofauna (Vanreusel et al., 1995; Gale´ r- 1995), the vertical sediment profile of nematode on et al., 2001; Iken et al., 2001). The low nematode densities was studied. As was discussed in the study and copepod densities at 5000–5500 m depth (Mol- by Pfannkuche and Thiel (1987), who focused on loy Hole), compared to stations at shallower depths the Barents Sea continental margin, mean relative with comparable Chl a and phaeopigment data, but nematode abundances in the first 2 cm of the higher FDA values, might confirm this, although sediment increase with water depth and with decreas- the lower quality of the organic material at greater ing nematode densities. The absolute nematode ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 121

1200 m 1500 m 3500 90 3500 90

3000 80 3000 80 70 70 2500 2500 60 60 2000 50 2000 50 1500 40 1500 40 30 30 1000 1000 20 20 500 10 500 10 0 0 0 0 2000 2001 2002 2003 2004 2000 2001 2002 2003 2004 year year

2000 m 2500m 3500 90 3500 90

3000 80 3000 80 70 70 2500 2500 60 60 2000 50 2000 50 1500 40 1500 40 30 30 1000 1000 20 20 500 10 500 10 0 0 0 0 2000 2001 2002 2003 2004 2000 2001 2002 2003 2004 year year

3000 m 3500 m 3500 90 3500 90 2 nem/10 cm 80 80 3000 2 3000 cop/10 cm 70 70 2500 2500 60 60 2000 50 2000 50 1500 40 1500 40 30 30 1000 1000 20 20 500 10 500 10 0 0 0 0 2000 2001 2002 2003 2004 2000 2001 2002 2003 2004 year year

4000 m 5000 m 3500 90 3500 90

3000 80 3000 80 70 70 2500 2500 60 60 2000 50 2000 50 1500 40 1500 40 30 30 1000 1000 20 20 500 10 500 10 0 0 0 0 2000 2001 2002 2003 2004 2000 2001 2002 2003 2004 year year 5500 m 3500 90

3000 80 70 2500 60 2000 50 1500 40 30 1000 20 500 10 0 0 2000 2001 2002 2003 2004 year

Fig. 8. Nematode and copepod density time series per depth. ARTICLE IN PRESS 122 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129

Stress:0.07 1000 1500 Thiel, 1987), even at deeper stations. In the study by 1000m-2000m 3000m-5500m Soltwedel et al. (2003), the occurrence of high 2000 2500 nematode abundances in deeper sediment layers in

3000 3500 the Molloy Hole is explained by a high predation pressure by dense herds of holothurians, dominat- 4000 5000 ing the epibenthos at 5600 m depth and intensively

5500 reworking the upper few millimeters of the sediment. Nematodes would be able to escape predation by vertical migration into deeper sediment horizons. This may explain the high relative abundances of Stress:0.07 the nematodes in deeper sediment layers at 2000 5000–5500 m depth.

2001 4.3. Time series 2002 Long-term studies are essential in order to 2003 understand better how benthic systems behave on ecological time scales. However, time-series in areas 2004 that are not easily accessible, such as the Arctic, are extremely scarce (Gooday, 2002). Fig. 9. MDS plot based on meiofauna taxa densities with indication of (A) different depths and (B) different years. A comparison of benthic data obtained in different years is affected by seasonal variability, because the timing, amount and composition of the annual sedimentation of phytodetritus as the major densities in the upper sediment layer do not vary a food resource for benthic organisms and the related lot between depths in contrast to the relative response of the benthos can vary considerably proportion of the nematodes inhabiting the upper (Fortier et al, 2002; Soltwedel et al., 2005). The centimeter, which increases with depth. The higher interannual variation of vertical flux in the Barents total nematode abundances (5-cm depth) at shallow Sea is determined by the dynamics of the inflowing stations, and also in the Molloy Hole, therefore, are warm, nutrient-rich Atlantic Water, which deter- caused by higher nematode densities in deeper mines the extent of ice cover and imports variable sediment layers. This observation, in addition to amounts of overwintering zooplankton (Slagstad the fact that densities are correlated with bacterial and Wassmann, 1991, 1997). Estimations of the activity (FDA) rather than with indicators for average annual vertical export of POC in the phytodetritus input, suggests that the meiofauna Barents Sea can vary from 17 g cm2 during cold and nematodes in particular are not the first order years to 39 gcm2 in warm years (Slagstad and consumers of the surface organic input. They rather Wassmann, 1997). The Fram Strait region, where respond when demineralization is already at an the HAUSGARTEN is located, is also well known advanced stage, as shown by earlier evidence from for large interannual fluctuations in local ice cover- stable isotope analyses at the Porcupine Abyssal age, and the intensity of the ice-edge blooms Plain (Iken et al., 2001). Also, in the study of (Sakshaug and Skjoldal, 1989). The bloom devel- Vanreusel et al. (1995), the vertical distribution of opment, the secondary production and the fate of nematodes in the sediment could be explained by a the organic matter along the west Spitzbergen and combination of bacterial densities and oxygen east Greenland shelf, however, are not known as supply. well as they are for the Barents Sea (Wassmann, In addition to food availability in deeper layers, 2002). also competition and predation pressure might be This study demonstrated a significant inter- responsible for the observed depth profiles in the annual variability in the meiobenthos and pigment sediments (Pfannkuche and Thiel, 1987; Soltwedel data at the HAUSGARTEN site between the years et al., 2003). Oxygen availability in subsurface layers 2000 and 2004. Because, firstly, no consistent is unlikely to be a limiting factor for the meiofaunal pattern was found in pigment data and, secondly, abundances in the arctic deep-sea (Pfannkuche and there was no correlation found between meiofauna ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 123

1200m 1500m 1 1

2 2

3 3

4 4 depth within the sediment (cm) depth within the sediment (cm) 5 5 0 200 400 600 800 1000 1200 0 200 400 600 800 1000 1200 Nematodens/10 cm2 Nematodens/10 cm2

2000m 2500m 1 1

2 2

3 3

4 4 depth within the sediment (cm) 5 depth within the sediment (cm) 5 0 200 400 600 800 1000 1200 0 200 400 600 800 1000 1200 Nematodens/10 cm2 Nematodens/10 cm2 3000m 3500m 1 1

2 2

3 3

4 4 depth within the sediment (cm) depth within the sediment (cm) 5 5 0 200 400 600 800 1000 1200 0 200 400 600 800 1000 1200 Nematodens/10 cm2 Nematodens/10 cm2

4000m 5000m 1 1

2 2

3 3

4 4

depth within the sediment (cm) 5 depth within the sediment (cm) 5 0 200 400 600 800 1000 1200 0 200 400 600 800 1000 1200 Nematodens/10 cm2 Nematodens/10 cm2 5500m 1

2 2000 3 2001 2002 2003 4 2004

depth within the sediment (cm) 5 0 200 400 600 800 1000 1200 Nematodens/10 cm2

Fig. 10. Nematode densities over the 5-cm depth proﬁle for each depth along the bathymetric transect. ARTICLE IN PRESS 124 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 Phaeopigments (0–2 cm) Phaeopigments (0–1 cm) 0.53 0.01 7 7 0.04–4.12 0.04 0.01–0.13 a 7 7 7 Chl (0–5 cm) a Chl (0–2 cm) a Chl (0–1 cm) MUC+BC MUC gear 1000 m BC 0.31 1000 m MUC 0.28–2.48 2.27–6.04 o o 5000 m 0.03–0.09 0.03–0.25 2.40–11.15 1000 m MUC 0.07–0.21 2.57–3.28 3000–4000 m4 500 3000–4000 m 0.017–0.183 0.05–0.25 1.049–7.40 0.03 2000–3000 m3000–4000 m1000–2000 m MUCo 2000–3000 0.021–0.067 m 0.09–0.561000–2000 m 0.01–0.09 BC3000–4000 m4000–5000 m 0.01–0.63 0 0.167–0.403 0–0.001 0.77–3.77 0 0.30–1.29 0.82–3.62 0.041–0.145 0.022–0.104 0.012 1000–2000 m MUC500 0.02 1.05 Pfannkuche and Thiel (1987) Schewe (2001) Schewe and Soltwedel (2003) Clough et al. (1997) Vanreusel et al. (2000) Schewe and Soltwedel (1999) Vanaverbeke et al. (1997) 0.02Soltwedel et al. (2000) 3000–4000 m 0.02 0.54 cm Depth Sampling 2 , phaeopigment and sampling gear data for different arctic regions a g/cm Hausgarten(1000 m–5500 m)NO–Svalbard (2500 m–3920 m) This study 1000–2000 m MUC 2000–3000 m 0.04–0.46 2000–3000 m 0.01–0.16 0.10–1.16 0.07–0.23 3.014–12.58 3.162–9.66 0.69 (481 m–4268 m)Central Arctic (1270 m–3170 m)Arctic Ice Margin (744 m–3020 m)Arctic (1000 m–4190 m)Central Arctic Central Arctic (864 m–4187 m) 1000–2000 m 2000–3000 m 1000–2000 m 0.14–1.07 2000–3000 m 0.006–0.036 0.03–0.95 0–0.001 0.67–5.25 0.102–0.139 1.30–5.63 0.017–0.051 Yermak Plateau Laptev Sea (1935 m–3237 m) 2000–3000 m 0.01 1.06 m Table 4 Chl ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 125

3500 nem (this study) nem centre arc 3000 nem laptev nem sval nem ant 2500 nemdens yermak 2

2000

1500 nem dens/10 cm 1000

500

0 0 1000 2000 3000 4000 5000 6000 depth (m)

90 cop (this study) 80 cop centre arc cop sval cop yermak 70

2 60

cop dens/10 cm 30

0 0 1000 2000 3000 4000 5000 6000 depth (m)

Fig. 11. Comparison nematode and copepod densities (ind/10 cm2) in different polar regions. Data are from the Central Arctic Ocean (nem/cop centr arc; Schewe and Soltwedel, 1999, Vanreusel et al., 2000, Schewe, 2001), the Laptev Sea (nem laptev; Vanaverbeke et al., 1997), the continental shelf of NE-Svalbard (nem/cop sval; Pfannkuche & Thiel, 1987), the Antarctic Weddel Sea (nem ant; Vanhove et al., 1995) and the Yermak plateau (nem/cop yermak; Soltwedel et al., 2000). densities and sediment-bound chloroplastic pig- different stage of the bloom growth cycle. This cycle ments, it was thought that following factors might consists of a pre-bloom phase with a minute hamper a sound interpretation of the data. Firstly, standing stock of phytoplankton, an exponential Gooday (2002) emphasizes the difficulty of sam- phase, a peak phase, a phase of decrease in standing pling the benthic community at the right time to stock, and a post-bloom phase that lasts till the re- document the short-term responses to flux events. freezing of the sea water (Sakshaug and Skjoldal, The time period between the start of the bloom and 1989). Sinking rates of the primary production the sampling is unknown in this study. The appear to be particularly high at the end of a bloom. phytoplankton bloom might, therefore, be at a At this time, the algae appear to be susceptible to ARTICLE IN PRESS 126 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 attack by bacteria (Sakshaug and Skjoldal, 1989), correlation with FDA. If nematodes rely on the which may also serve as an important food source microbial loop to stimulate their production (Flee- as shown in this study. The different stages of the ger et al., 1989), one might indeed not expect rapid phytoplankton bloom are also dominated by a nematode density changes but time lags between different phytoplankton community (Olli et al., sedimentation of surface organic matter and nema- 2002; Drinkwater et al., 2003). Therefore, both tode density increases. quantity and quality of the food reaching the Fleeger et al. (1989) provided further reasons for bottom changes during the phytoplankton growth the lack of correlations between the benthos cycle. Differences in the stage of the phytoplankton densities and food input. The role of reproduction, bloom growth cycle may cause the differences in the predation, and winter survivorship as factors sediment bound chloroplastic pigments found in regulating species abundances could influence over- this study. The lack of correlation between sediment all benthos densities. Finally, yearly variation in bound chloroplastic pigments and meiofauna den- sedimentation may even not be great enough. This, sities could then be explained by the differences in however, seems unlikely, as food availability at the quality of the material and amount of bacteria HAUSGARTEN varies as much in time as it does accompanying the organic matter. The %Chl a, along the bathymetric gradient and along this however, could not explain the differences in gradient, differences in food availability are re- meiobenthos densities. flected in the meiobenthos densities. Secondly, the relation between what is produced The highest variations in nematode and copepod at the sea surface and what reaches the bottom is densities over time were observed at 2000 m and very complex. The zooplankton can considerably even more at 2500 m water depth. Unlike those at alter the flux of organic matter both in a positive shallower depths, meiofauna at these two stations way (production of fast-sinking fecal pellets) and a may be limited by food quantity and quality. As a negative way (very high grazing rates) (Wassmann, result, they are likely to respond in a more obvious 1998; Olli et al., 2002; Fortier et al., 2002; Hansen way to interannual or seasonal variations in sea ice et al., 2003). This means that the pigments found on conditions, primary production and corresponding the ocean bottom do not always reflect the surface food inputs to the seafloor. Food quality at deeper primary production. Because the spatial distribution stations may be so low that nematode communities of the zooplankton community can vary consider- are unable to benefit from a considerable increase in ably along the MIZ (Wassmann, 1998; Olli et al., food quantity, whereas at shallower stations, food 2002; Fortier et al., 2002; Hansen et al., 2003) this quality and quantity are high enough even in years could explain why no consistent pattern in meio- with lower food availability. fauna densities and sediment-bound chloroplastic The high temporal variability in the vertical pigments for each separate year could be found. distribution of nematodes in the sediment at Another point to emphasize is that seasonal shallower depths along the bathymetric gradient organic-matter inputs make an important contribu- may indicate that nematodes at these depths react to tion to the spatial heterogeneity of the ocean-floor increased input of organic matter by migrating environment. This means that in practice it is deeper into the sediment (Gale´ ron et al., 2001). difficult to distinguish between temporal variability Enhanced food availability is normally reflected in and spatial patchiness (Gooday, 2002). It should be the vertical distribution of the organic compounds noted though that in this study samples come from in the sediment column (Soltwedel et al., 2000). just one MUC haul per station and year. This could Bioturbating macrofaunal organisms induce a rapid minimize the spatial patchiness among stations downward mixing of the organic matter (Witte (Hurlbert, 1984). Differences between the years et al., 2003) making it available deeper in the could, therefore, be due to patchiness induced by sediment. At deeper stations nematodes may be heterogeneous distribution of food to the seafloor obliged to inhabit the upper centimeters of sediment (Gage, 1996; Levin et al, 2001). as deeper layers are depleted in food. Here again, Also, nematodes might not depend on the however, we found no correlation between propor- primary production itself but on the bacteria tional nematode densities in the upper 2 centimeters accompanying this material. The results of this of the sediment and sediment bound chloroplastic study suggest that the abundance of bacteria is pigments, and even no correlation with FDA. There related to nematode densities, which show a positive is no information available from the study sites ARTICLE IN PRESS E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129 127 about macrofauna densities, predation pressure and References bioturbation, factors which may also help to regulate the depth profiles. Beaulieu, S.E., 2002. Accumulation and fate of phytodetritus on the seafloor. Oceanography And Marine Biology—An Annual Review 40, 171–232. 5. Conclusions Billett, D.S.M., Lampitt, R.S., Rice, A.L., Mantoura, R.F.C., 1983. Seasonal sedimentation of phytoplankton to the deep sea. Nature 302, 520–522. The results of this study suggest the following Clarke, K.R., 1993. Non-parametric multivariate analyses of answers to the questions posed in the Introduction. changes in community structure. Australian Journal of Ecology 18, 117–143. Clarke, K.R., Warwick, R.M., 1994. Change in Marine Com- (1) The high productivity along the The Marginal munities: An Approach to Statistical Analysis and Interpreta- Ice Zone is reflected in high meiobenthos tion. Plymouth Marine Laboratory, Plymouth, UK, pp. 144. densities. Clarke, K.R., Gorley, R.N., 2001. Primer v5: User Manual/ (2) The topography of the HAUSGARTEN region Tutorial. PRIMER-E. Plymouth Marine Laboratory, Ply- divides the bathymetric gradient into two dis- mouth, UK, pp. 91. tinct areas based on environmental variables as Clough, L.M., Ambrose, W.G., Cochran, J.K., Barnes, C., Renaud, P.E., Aller, R.C., 1997. Infaunal density, biomass well as meiofauna densities. and bioturbation in the sediments of the Arctic Ocean. Deep- (3) Meiofauna densities and vertical depth profiles do Sea Research II 44, 1683–1704. change over time, especially at 2000 and 2500 m Drinkwater, K., Belgrano, A., Borja, A., Conversi, A., Edwards, depth, but no consistent pattern could be found. M., Greene, C., Ottersen, G., Pershing, A., Walker, H., 2003. The lack of knowledge about spatial patchiness, The response of marine ecosystems to climate variability associated with the North Atlantic Oscillation. In: Hurrell, J., interannual variations in intensity of the bloom, Kushnir, Y., Ottersen, G., Visbeck, M. (Eds.), The North zooplankton communities and time lags in Atlantic Oscillation: Climatic Significance and Environmental response to increased food input hamper a sound Impact, vol. 134. American Geophysical Union, Washington, interpretation of inter-annual variations. DC, pp. 211–234. (4) The variation in microbial production is prob- Engelsen, O., Hegseth, E.N., Hop, H., Hansen, E., Falk-Petersen, ably the most important factor structuring S., 2002. Spatial variability of chlorophyll-a in the Marginal Ice Zone of the Barents Sea, with relations to sea ice and meiobenthos communities in time and over oceanographic conditions. Journal of Marine Systems 35, water- and sediment depth. 79–97. Falk-Petersen, S., Hop, H., Budgell, W.P., Hegseth, E.N., Acknowledgements Korsnes, R., Løyning, T.B., Ørbæk, J.B., Kawamura, T., Shirasawa, K., 2000. Physical and ecological processes in the marginal ice zone of the northern Barents Sea during the The first author acknowledges a grant (2002–06) summer melt period. Journal of Marine Systems 27, 131–159. from the Institute for the Promotion of Innovation Findlay, R.H., King, G.M., Watling, L., 1989. Efficiency of through Sciences and Technology in Flanders phospholipids analysis in determining microbial biomass in (IWT-Vlaanderen). This study is part of the multi- sediments. Applied Environmental Microbiology 55, disciplinary research at the HAUSGARTEN site 2888–2893. coordinated by the Alfred-Wegener Institute for Fleeger, J.W., Shirley, T.C., Ziemann, D.A., 1989. Meiofaunal responses to sedimentation from an Alaskan spring bloom. I. Polar and Marine Research. This research was Major taxa. Polar Biology 57, 137–145. supported by the HERMES project, EC contract no Fortier, M., Fortier, L., Michel, ., Legendre, L., 2002. Climatic GOCE-CT-2005-511234, funded by the European and biological forcing of the vertical flux of biogenic particles Commission’s Sixth Framework Program under the under seasonal Arctic ice. Marine Ecology Progress Series priority ‘Sustainable Development, Global Change 225, 1–6. Gage, J., Tyler, P., 1991. Deep Sea Biology: a Natural History of and Ecosystems’. We would like to thank the Organisms at the Deep Sea Floor. Cambridge University Alfred-Wegener Institute for Polar and Marine Press, Cambridge, pp. 504. Research, the captain, crewmembers, and chief Gage, J.D., 1996. Why are there so many species in deep-sea scientists of the research vessel R.V. Polarstern for sediments. Journal of Experimental Marine Biology and providing the samples. Also a special thanks to Bart Ecology 200, 257–286. Beuselinck for the extraction of the meiofauna. We Gale´ ron, J., Sibuet, M., Vanreusel, A., Mackenzie, K., Gooday, A.J., Dinet, A., Wolff, G.A., 2001. Temporal patterns among are thankful to the anonymous reviewers and the meiofauna and macrofauna taxa related to changes in editor for their constructive comments on this sediment geochemistry at an abyssal NE Atlantic site. manuscript. Progress in Oceanography 50, 303–324. ARTICLE IN PRESS 128 E. Hoste et al. / Deep-Sea Research I 54 (2007) 109–129

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