Benthic Organic Matter Supply and Metabolism at Depositional and Non-depositional Areas in the North Sea

Estuarine, Coastal and Shelf Science (1999) 49, 747–761 Article No. ecss.1999.0555, available online at http://www.idealibrary.com on

Benthic Organic Matter Supply and Metabolism at Depositional and Non-depositional Areas in the North Sea A. R. Boona, G. C. A. Duineveldb and A. Kokb a

Netherlands Institute for Fisheries Research, Department of Biology and Ecology, P.O. Box 68, 1970 AB IJmuiden, The Netherlands b Netherlands Institute for Sea Research, Department of Marine Ecology, P.O. Box 59, 1790 AB Den Burg, The Netherlands Received 2 October 1998 and accepted in revised form 21 July 1999 In 1994, four stations in the southern North Sea, the German Bight and the Skagerrak were visited with the aim to get insight into spatial and temporal variation in the supply of fresh organic matter to the benthos and its subsequent metabolic reaction. Stations were chosen on the basis of differences in sediment type, depth and depositional regime. Sediments were sampled, sliced and analysed for phytopigments, fatty acids and nucleic acids. On-deck sediment core incubations provided the sediment oxygen demand (SOD). Fatty acids as well as chlorophyll a indicated a seasonal variation of phytodetritus sedimentation, with highest values in May, reflecting the spring bloom sedimentation. The two stations in the depositional areas German Bight and Skagerrak had the highest input of algal detritus into the sediment. These stations also contained higher concentrations of bacterial and long-chain fatty acids, probably related to the relatively higher proportion of fine particles in the sediment and to the input of terrestrial organic matter and/or refractory marine organic matter, respectively. The metabolic indices, viz. the SOD and the RNA concentrations reflected the benthic metabolic reaction to the labile organic matter supply. The three stations in the southern and south-eastern North Sea had a SOD congruent with the phytodetrital inventories, with highest SOD measured at the German Bight. Surprisingly, the Skagerrak sediment did not have a high oxygen demand, although it contained the highest inventory of labile organic matter and high RNA concentrations. The fluxes of carbon to the sediment at station SK, calculated from the chlorophyll a inventory, were about four times higher than the sediment oxygen demand. We hypothesise two mechanisms for this discrepancy; one is the decreased mineralisation rate of labile organic matter due to sorption to clayey sediment particles, the other is advection of labile organic matter from the shallower coastal waters of northern Denmark to and subsequent removal from the deeper Skagerrak sediments by periodically occurring high near-bottom water currents.  1999 Academic Press Keywords: benthic-pelagic coupling; sediment; SOD; chlorophyll; fatty acids; RNA; degradation; North Sea

Introduction The close relationship between detrital supply to sediments and benthic metabolism has been demonstrated in the deep sea (Smith Jr, 1978; Thiel et al., 1988/1989) as well as continental seas (Smetacek, 1984; Kanneworff & Christensen, 1986; Boon et al., 1998). Boon and Duineveld (1998) demonstrated an annual balance between the amount of fresh detrital carbon supplied to and mineralized in the sediments of the southern and central North Sea. Although the sites in the latter study were all located in nondepositional areas (i.e. without long-term deposition of fine particles) in the North Sea, a substantial part, up to 40%, of primary production was buried and subsequently degraded in these sediments. In this context, the role of depositional areas in benthic organic matter cycling within the North Sea is 0272–7714/99/110747+15 $30.00/0

unclear. Are such areas, which are sinks for fine mineral particles and refractory carbon, also sinks for labile organic matter? How do these areas compare to non-depositional areas with regard to the nature and amount of detritus and its mineralisation within sediments? Other benthic studies of these depositional areas in the North Sea have measured nutrient fluxes (Lohse et al., 1995) and bacterial production (Van Duyl & Kop, 1994). However, studies of the amount and nature of labile organic matter in recent sediments in the North Sea are scarce and limited to certain areas (Liebezeit, 1987; Kempe & Jennerjahn, 1988; Wiesner et al., 1990; Anton et al., 1993). Moreover, they were not accompanied by benthic metabolic measurements. To gain insight into the above questions, this study focused on the sediment detritus composition and  1999 Academic Press

748 A. R. Boon et al.

benthic metabolism in depositional and nondepositional areas during three cruises in 1994 at four locations in the southern and eastern North Sea. Stations were chosen based on their depositional environment, depth and the possible different origins of recent organic matter. Two stations were selected in acknowledged depositional areas, i.e. the German Bight and the Skagerrak (Eisma & Kalf, 1987a; De Haas et al., 1997; Puls et al., 1997). For comparison, the other two stations were located in nondepositional areas in the southern North Sea. These stations, at the Broad Fourteens and the Frisian Front, have been studied relatively extensively with regard to the supply of phytodetritus to the sediments and congruent benthic metabolism (Duineveld & Jenness, 1984; Creutzberg, 1985; Jenness & Duineveld, 1985; Cramer, 1990; Boon & Duineveld, 1996; Boon et al., 1998). The nature and concentration of sedimentary labile organic matter were determined by analyses of phytopigments and fatty acids. Phytopigments have been widely used as markers for biomass and composition of algae in the water column (Lorenzen, 1967; Gieskes & Kraay, 1983). Since the major source of fresh organic matter in most benthic habitats consists of phytodetritus, phytopigments represent obvious markers for benthic food input (Gillan & Johns, 1980; Relaxans et al., 1992). There have been numerous studies where the sedimentation of detritus on the seabed has been successfully traced by means of pigments even at the deep-sea floor (Billett et al., 1983; Rice et al., 1986; Duineveld et al., 1997). Chlorophyll a, present in all algae and some photosynthetic bacteria, appears to be a good proxy for the labile organic matter pool (Stephens et al., 1997; Boon & Duineveld, 1998). Therefore, in this study, chlorophyll a is used to follow the temporal and spatial input of phytodetritus to North Sea sediments. Fatty acids are important lipid components in all organisms. Their main roles are in cell membranes and energy storage, but they also have a physiological function as hormone precursors (Sargent et al., 1990; Stanley & Howard, 1998). Since bacteria, algae and terrestrial plants have different biosynthetic pathways for fatty acids, these organism groups can, to some extent, be discriminated by their fatty acid compositions (Gurr & James, 1980; Arao & Yamada, 1994). Due to their specificity and the fact that they are relatively short-lived, fatty acids are important markers for the origin and nature of labile organic matter in water and sediments (Saliot et al., 1982; Reemtsma et al., 1990; Santos et al., 1994; Wolff et al., 1995; Boon & Duineveld, 1996). This study provides the first description of fatty acid

concentrations and their composition in recent North Sea sediments. The metabolic response of the whole benthic community was measured using sediment oxygen consumption (Smith Jr, 1978; De Wilde et al., 1984). Furthermore, we measured the sedimentary RNA and DNA concentration. In earlier studies, the ratio of these components has been used for assessing the metabolic activity of cultured bacteria (Kerkhof & Ward, 1993; Kemp et al., 1993) and metazoan organisms (Dortch et al., 1983; Mayrand et al., 1995). However, Kemp et al., (1993) suggested that RNA is a better indicator for bacterial activity than the RNA and DNA ratio. Danovaro et al. (1993) used this ratio to indicate sedimentary metabolism, but regarding this, their results were not convincing. Moreover, other studies have indicated that especially DNA in sediments is at least partially detrital (Dortch et al., 1983; Dell’Ano et al., 1998). Considering the above, we used only RNA as an additional metabolic proxy. Methods Description of study sites Two non-depositional stations were selected in the southern North Sea, station Broad Fourteens (BF) and station Frisian Front (FF) (Figure 1). The third station is located in the German Bight (GB) and the last station is situated in the Skagerrak (SK), respectively in the south-eastern and north-eastern North Sea and are both depositional areas (Figure 1). An overview of some characteristics of the stations is given in Table 1. Station BF (c. 30 m depth) has a sandy bottom which is poor in organic carbon (Corg), and has relatively high near-bottom current velocities (max. c. 45 cm s
1; Boon & Duineveld, 1996). Although fresh organic matter has been found in the sediments (Jenness & Duineveld, 1985; Boon et al., 1998), no net deposition of particulate matter takes place (De Haas et al., 1997). More likely, it is a site with net erosion of sediments (Eisma & Kalf, 1987a). At station FF, at c. 40 m depth, near-bottom currents are lower than at station BF, max. 25 cm s
1 (Boon unpubl. data), while the sediment consists of a mixture of fine sand and silt with an Corg content c0·5% (De Haas et al., 1997). It is situated in a frontal area of two converging water masses, i.e. one that enters the North Sea from the south through the channel, the other from the north around Scotland. Primary production at stations FF is often prolonged after the spring bloom and the sediment contains enhanced levels of phytodetritus compared to stations to the north and south (Creutzberg, 1985; Baars et al.,

Benthic supply and metabolism in the North Sea 749

Norway

Skagerrak N

Denmark

German Bight

Frisian Front

Broad Fourteens Germany Netherlands United Kingdom

Belgium

F 1. Map North Sea with sample sites. T 1. Some characteristics of the sample locations in this study

Station Broad Fourteens Frisian Front German Bight Skagerrak

Latitude (, N) 53, 53, 54, 58,

00 42 05 12

Longitude (, E) 3, 4, 8, 10,

52 30 09 15

Depth (m)

Mixing

Sediment type

Corg (% in sed.)

28 39 20 270

Mixed Transitional Mixed Stratified

Medium coarse sand Fine sand and silt Silt and fine sand Silt

0·01–0·05 0·05–0·5 1–2 1·5–2

1991). The local enrichment of station FF with labile organic matter is also apparent from the increased benthic biomass and sediment oxygen consumption (Creutzberg, 1985; Cramer, 1990; Boon et al., 1998). At the third station, GB, near-bottom current velocities are close to those at station BF (Boon &

Duineveld, 1996). Nevertheless, the sediment contains a relatively high concentration of Corg (1–2%) and silt. As a result of a net inflow of suspended matter and local eddy-formation, it is considered a depositional area (Eisma, 1987; Puls et al., 1997). The sedimentation rate in this area could not be determined due to high bioturbation activity (De

750 A. R. Boon et al.

Haas et al., 1997). The last station, SK, is situated at the southern slope of the Skagerrak and is considerably deeper than the other stations, c. 270 m. Nearbottom currents vary between 5 and 10 cm s
1, although temporarily higher current velocities can occur (Svansson, 1975). At this sampling site, the sediment consists of clayey and sandy silts, with a Corg content in the top layer between 1·5 and 2% (De Haas, 1997) and the annual sedimentation rate in the area varies between 2 and 4 mm (see De Haas & Van Weering, 1997). This area is believed to be the ultimate sink for about half of the refractory carbon produced in the North Sea. Calculations indicate that about 106 tonnes of organic matter accumulate annually in the Skagerrak/northern Kattegat, of which 90% is imported (De Haas & Van Weering, 1997). This is at least 10 times the organic matter buried in the North Sea (De Haas et al., 1997) and underlines the importance of the Skagerrak area as a carbon sink. Sampling and analytical procedures The four sampling sites were visited with the RV Pelagia at 14 to 24 February, 24 to 31 May and 15 to 31 August 1994. Prior to sampling, a CTD cast was performed on each site, with a fluorometer, a transmissometer (Sea-Tech, beam length 025 m, wavelength 660 nm) and Niskin bottles attached to the frame. The fluorometer and the transmissometer were not calibrated, and thus give only a relative indication of the concentrations of total suspended matter and chlorophyll a in the water column at the sample stations. The near-bottom water (c. 3 m above bottom) was analysed for oxygen concentration by Winkler titration. Sediment samples were taken with a cylindrical boxcorer (B 31 cm), which encloses a 30 to 50 cm long sediment column together with 15 to 24 l of overlying bottom water. Disturbance of the sampled sediment–water interface and intrusion of overlying water is prevented by a tightly sealing top valve. For the phytopigment and fatty acid analyses, multiple sediment cores (10 cm length) were taken from different box cores with 50 ml cut-off syringes. For the nucleic acid analyses, the sediment was sampled with 10 ml cut-off syringes (8 cm length). Samples were directly frozen in liquid nitrogen, after which they were stored at
80 C until processing in the laboratory. There, the frozen samples were sliced in sections of 0 to 1, 1 to 2, 2 to 3, 3 to 5, 5 to 7 and 7 to 10 cm for phytopigment and fatty acid analyses, and in sections of 0 to 0·5, 0·5 to 1, 1 to 2, 2 to 3, 3 to 4 and 4 to 6 cm for the nucleic acid analyses. Prior to analyses, the sediment samples were lyophilized. Phytopigment analyses were performed on

duplicate samples by reverse-phase high-performance liquid chromatography (RP-HPLC), using the methodology described in Boon et al. (1998). To reduce the amount of fatty acid analyses, only the sediment sections of 0 to 1, 2 to 3 and 5 to 7 cm depth were processed, and one core per sampling station per sampling event was analysed. Fatty acids were extracted according to Boon et al. (1975), with minor modifications. Analyses were performed by gas chromatography (GC) and identification of individual compounds was carried out by gas chromatography– mass spectrometry (GC-MS). More information on the analytical procedure concerning fatty acid analyses is given in Boon and Duineveld (1996). Nucleic acids in the sediment samples (no replicates) were analysed by injecting an extract into an HPLC-system equipped with a Nucleogen 4000-7 DEAE anion exchange column (Machery-Nagel). The analytical procedure is extensively described in Stoeck et al. (1998). A study comparing methods for RNA and DNA extraction and quantification, and including the one used in this study, showed it to be very comparable to other methods for RNA and DNA quantification (Dell’Ano et al., 1998). Sediment oxygen demand (SOD), which covers the rate of aerobic respiration of the sediment community and partly the oxidation of reduced substances as well (Canfield et al., 1993), was measured in shipboard incubated sediment cores (two to four replicates). Detachable polyester cores (B 30 cm) were inserted in the cylindrical box corer described above. On deck, the core tubes were placed into a water bath with an opaque lid to prevent light from entering. A heightadjustable lid was fitted into each core tube by means of an inflatable ring in the outer rim, allowing adjustment of the water volume in the core. Using an external pump and cooling device, the water surrounding the cores was cooled to in situ temperature. The lid held a stirring device and an oxygen electrode (Yellow Spring Instruments 620) to monitor the oxygen concentration in the head space. The electrode was calibrated in aerated, oxygen-saturated water (100% O2), and in oxygen-depleted (sodium sulphite) water (0% O2). SOD was estimated from the linear part of the first 2 to 3 hours of the concentration-time series. The sediment oxygen demand was corrected for the oxygen use by the electrode in filtered seawater, containing no organic matter. Anova with Tukey’s HSD test were used to check on significant differences between stations and times of sampling. Relations between marker compounds or compound groups were calculated with Pearson correlations. All statistical calculations were carried out using Systat for Windows.

Benthic supply and metabolism in the North Sea 751 T 2. Overview of near-bottom water characteristics measured by CTD, i.e. temperature (T; C), fluorescence (Fl; ìg chlorophyll a l
1), transmission (TR; % at 660 nm), oxygen content (O2 ìmol l
1) at the sampling stations in February, May and August 1994 February

BF FF GB SK

May

August

T

Fl

TR

O2

T

Fl

TR

O2

T

Fl

TR

O2

5·0 4·5 3·9 3·4

2·0 0·5 1·5 0·2

72 65 4 77

309 316 337 253

11·8 11·2 10·2 5·8

1·5 1·2 1·7 0·2

66 60 20 74

265 258 293 256

18·9 17·5 18·8 6·4

2·0 2·0 3·0 0·2

70 57 2 78

249 248 270 265

Sediment oxygen demand

3500 3000 2500 2000 1500 1000 500 0

* BF

FF

GB

SK

Stations

F 2. Sediment oxygen demand (ìmol m
2 h
1) at sample locations in February ( ), May ( ) and August ( ) 1994. *SOD value at BF taken from Boon et al. (1998). Error bars denote standard deviation.

Results Water column characteristics Table 2 summarizes the near-bottom water (nbw) temperature, chlorophyll a equivalents, transmission and the oxygen concentration in the nbw as measured with CTD-casts at the stations during sampling (see also Boon & Duineveld, 1996). The nbw temperature at the stations BF, FF and GB was lowest in February, between 3·9 and 5 C, and highest in August with a maximum between 17·5 and 18·9 C. At station SK, the bottom water temperature increased from 3·4 C in February to 6·4 C in August, Here, the water column showed multiple thermoclines and haloclines during each cruise (data now shown). Station FF exhibited a (weak) thermocline only in May, while the water column at the stations BF and GB was mixed on every cruise. At all stations and during each cruise, the nbw was well oxygenated.

Sediment oxygen demand The average sediment oxygen demand (SOD) data are shown in Figure 2. The highest SOD was consistently measured at the stations FF and GB (P<0·01) and the lowest values at station BF, with relatively low values at station SK in May and August. No measurements were possible in May at station BF due to technical problems. However, SOD measurements made at this station in May of previous years at this station (Van Duyl & Kop, 1994; Boon & Duineveld, 1998) varied around 370 (10) ìmol 02 m
2 h
1. Maximum SOD values at the station FF and SK were found in May, and at station GB in August (P<0·05). Pigment concentration and composition Figure 3 shows the inventories of chlorophyll a per cm2 sediment in the top 10 cm of the sediment. For

752 A. R. Boon et al. 9000 8000 7000 6000 Inventory

5000 4000 3000 2000 1000

SK Aug

SK May

SK Feb

GB Aug

GB May

GB Feb

FF Aug

FF May

FF Feb

BF Aug

BF May

BF Feb

400 300 200 100 0

Station, Month

F 3. Sediment inventories (0–10 cm) of chlorophyll a (100) ( ) and total fatty acids (ìg cm
2) ( ).

the calculation of these inventories, we converted the concentrations per gram into concentrations per cm3, using a specific density of 2·6 g cm
3, and an average porosity of 0·4, 0·53, 0·66 and 0·84 (Lohse et al., 1995; De Haas et al., 1997) at stations BF, FF, GB and SK, respectively. Although spatial and temporal trends in the inventories are obvious, ANOVA with Tukey’s HSD test yielded only few significant differences because of the heterogeneous replicate values of sedimentary chlorophyll a concentrations. Overall, highest concentrations were found in May, when months were compared, and at stations GB and SK, when stations were compared (months pooled; P<0·05). The chlorophyll a concentrations were lowest in February at station BF compared to all other stations (P<0·05) and highest at station SK in May compared to stations BF and FF (P<0·05). In the majority of the cores, chlorophyll a decreased with depth. A substantial number of cores showed a subsurface maximum, while in some cores the concentration of chlorophyll a was erratic or showed an increasing trend with depth. The latter profiles were mostly found in May. Figure 4 shows some characteristic down-core distributions of chlorophyll a and phaeopigment concentrations (phaeophorbides a and phaeophytins a). The down-core phaeopigment concentration was strongly related to that of chlorophyll a. Subsurface maxima in chlorophyll á concentration coincided with subsurface maxima in the phaeopigment concentration. However, in most cores the proportion of phaeopigments to the sum of phaeopigments and chlorophyll á increased with depth, re-

sulting in negative correlations between these two compounds in many cores (at stations BF, GB and SK: P<0·05). Fatty acid concentration and composition A total of 46 different fatty acids were identified when all the samples are considered. However, in order to present the data on the fatty acid concentration and composition in a comprehensible form, fatty acids were grouped according to their origin and/or nature of organic matter. Specific groups relate to the so-called bacterial, polyunsaturated, and terrestrial fatty acids. The first group (BACT) constitutes of isoand anteiso-branched C15:0 fatty acids, which are produced by gram-negative bacteria and many groups of gram-positive bacteria (Perry et al., 1979; Bobbie & White, 1980). Although the concentration of these fatty acids may differ per strain, it is generally assumed that the relative concentrations of these particular fatty acids in sediment gives an indication of the sedimentary bacterial biomass (e.g. Reemtsma et al., 1990). The PUFA (polyunsaturated fatty acid) group, produced by algae, consists of all fatty acids with two or more unsaturated bonds. The TERR group consists of saturated straight-chain fatty acids with chain lengths of 24 carbon atoms and longer. Cuticular waxes on terrestrial plant leaves are known to possess long-chain fatty acids and alkanes (Kolattukudy, 1976). Thus, the presence of long-chain fatty acids in sediments can indicate a terrestrial source of the sedimentary organic matter. However, certain algae

Benthic supply and metabolism in the North Sea 753 (a) 2

(b) 14

16

0

0–1

0–1

1–2

1–2

2–3 3–5

Depth (cm)

Depth (cm)

0

Concentration (µg g–1) 10 4 6 8 12

5

Concentration (µg g–1) 10 15 20

25

2–3 3–5

5–7

5–7

7–10

7–10

F 4. Depth distribution of chlorophyll a ( ) and phaeopigment ( ) concentrations (ìg g
1) in Skagerrak (a) and German Bight (b) sediments, August 1994.

are known to have relatively low amounts of the same compounds (Volkman, 1986). Due to a lower decay rate in comparison to their lower molecular weight counter parts, a part of the increase of the TERR to TFA ratio could also result from the preferential decay of the lower molecular weight fatty acids (Reemtsma et al., 1990). The inventories of TFA are shown in Figure 3. The inventory is calculated as with the pigments, with the assumption that the average fatty acid concentration of the selected core slices (0–1, 2–3, 5–7 cm depth) is representative for the average value of the total core down to 10 cm depth. This is a valid approach for an exponentially decreasing (‘ diffusive ’) concentration profile. However, when a non-local mixing event occurred in one of the slices that were not measured, this could introduce some error. In Figure 5, the PUFA values are given as a percentage of the TFA inventory per core. Major PUFA (>10% of TFA) in this study were C20:5 (a fatty acid of 20 carbon atoms long, with five double bonds) and C22:6, but in many cases C16:4, C16:3, C18:4, C18:3, C18:2, C20:4, C20:3 and C22:5 were also present. In coastal environments, PUFAs are uniquely synthesized by algae (DeMort et al., 1972; Viso & Marty, 1993; Dunstan et al., 1994), and are therefore markers for fresh algal detritus. Some copepod species also contain high concentrations of these compounds in their tissue, but this also originates from digestion and assimilation of algal material (St. John & Lund, 1996). Because the variation in the PUFA concentrations accounted for the largest part of the variation in the TFA concentrations (stations pooled: R2 =0·85), both groups show corresponding trends. Figure 3 and 5

clearly illustrate the strong similarity between the temporal and spatial variations of PUFA and chlorophyll a (R2d0·72, P<0·001): highest inventories at station SK, lowest at station BF, and intermediate inventories at stations FF and GB, with a seasonal maximum in May. The inventories of the BACT group did not show explicit temporal cycles (Figure 5). However, there are noticeable differences between stations with respect to BACT, comparable to those of chlorophyll a and TFA, i.e. increasing concentrations in the order of stations BF, FF, GB and SK (Pc0·06). When stations are pooled, we find a positive correlation between BACT and PUFA (R2 =0·53, P<0·01). If we express BACT as a percentage of TFA (Figure 6), differences between months and stations diminished. However, when each core is considered separately, there is no correlation between the downcore concentration of BACT on the one hand and that of PUFA or TFA on the other hand. While PUFA shows a decrease with depth in most cores, BACT does not show any consistent down-core pattern. Furthermore, when expressed as a proportion of TFA, BACT shows a negative correlation with the PUFA concentration (stations pooled: P<0·001). The inventories of the long-chain fatty acids (TERR) were relatively low at station BF and slightly higher at station FF (Figure 5). The other two stations, GB and SK, were distinguished by significantly higher concentrations of TERR (P<0·05; months pooled). When TERR is expressed as percentages of TFA (Figure 6), the differences between stations are still visible, although less

754 A. R. Boon et al.

Inventory, percentage of TFA

140 120 100 80 60 40

SK Aug

SK May

SK Feb

GB Aug

GB May

GB Feb

FF Aug

FF May

FF Feb

BF Aug

BF May

0

BF Feb

20

Station, Month

F 5. Sediment inventories (ìg cm fatty acids in sediment inventory.


2

) of bacterial ( ) and terrestrial fatty acids ( ) and percentage PUFA ( ) of total

Percentage of TFA

10

8

6

4

SK Aug

SK May

SK Feb

GB Aug

GB May

GB Feb

FF Aug

FF May

FF Feb

BF Aug

BF May

0

BF Feb

2

Station, Month

F 6. Percentages of bacterial ( ) and terrestrial fatty acids ( ) of total fatty acids in sediment inventories.

pronounced. Like BACT, also TERR shows a positive correlation with TFA and PUFA when all stations are considered, but not when calculated per station. Nucleic acids The inventories of both RNA and DNA displayed a comparable trend at all stations (Figure 7), with low values in February, highest concentrations in May and

intermediate concentrations in August. Especially in May and August, there were distinct differences between stations. As with the chlorophyll a and the fatty acids, station BF had the lowest RNA and DNA values, station FF showed intermediate concentrations, and the highest values were measured at the stations GB and SK. In general, the concentrations of RNA decreased with depth, though in some cores, a subsurface maximum was found.

Benthic supply and metabolism in the North Sea 755 450 400

Inventory (µg cm–2)

350 300 250 200 150 100 50

SK Aug

SK May

SK Feb

GB Aug

GB May

GB Feb

FF Aug

FF May

FF Feb

BF Aug

BF May

BF Feb

0

Station, Month

F 7. Sediment inventories (ìg cm
2) RNA ( ) and DNA ( ).

Discussion Phytodetrital supply The temporal trends in the inventories of chlorophyll a, total fatty acids and polyunsaturated fatty acids were comparable at all stations, with concentrations peaking in May. The proportions of PUFA in the total fatty acid concentrations also peaked in May, with percentages over 20% compared to <10% in February. This is consistent with the timing of the algal spring bloom in the North Sea, which usually takes place late April or early May (Joint & Pomroy, 1993), and which has a pronounced effect on the inventory of chlorophyll a in the sediments (Cramer, 1990; Boon et al., 1998). Differences between the stations in sedimentary chlorophyll a concentrations could only be proven significant (P<0·05) in the case of stations GB and SK. Because the spatial trends in chlorophyll a are paralleled by those in PUFA and TFA concentrations, there is enough support to rank the station regarding input of fresh phytodetritus as BF
ation in the sediment around slack tide (Jenness & Duineveld, 1985; Boon unpubl. data). Some of the input could be due to intrusion of small detrital particles in the coarse sediments during relatively high nbw currents (Hu¨ttel et al., 1996). The differences we found between the chlorophyll a inventories at station BF and at station FF are in line with previous studies. The relative detrital enrichment of sediments at station FF is due to an enhanced and prolonged primary production caused by the presence of a tidal front in the area of station FF in combination with lower nbw-current velocities, maximum 25 cm s
1 (Creutzberg, 1985; Boon & Duineveld, 1998). Our data on TFA and especially on PUFA concentrations support the contention that the sediment at station FF receives a greater supply of labile algal detritus than at station BF (Creutzberg et al., 1984; Duineveld et al., 1990; Cramer, 1990; Boon et al., 1998). The chlorophyll a and PUFA inventories at station GB are equal to or surpass those at station FF in spite of the higher nbw current velocities at station GB (max. c. 40 cm s
1; Boon & Duineveld, 1996). The explanation for this is two-fold. Firstly, the algal biomass in the German Bight is the highest in the range found in the southern North Sea (Joint & Pomroy, 1993), as a result of fluvial enrichment (Elbe, Weser) of nutrients (Radach et al., 1990; Bauerfeind et al., 1990). Secondly, sedimentation of particulate matter in the German Bight is promoted by the local hydrographic conditions, i.e. a higher supply of particulate material during flood than is removed during

756 A. R. Boon et al.

ebb and a counter-clockwise eddy, which retains suspended material (Eisma & Kalf, 1987b; Otto et al., 1990). Puls et al. (1997) calculated a net-deposition of particulate matter in the German Bight of 3 106 ton yr
1, about a tenth of what Van Weering et al. (1987) calculated for the Skagerrak based on 210 Pb geochronology. An unexpected result is our finding that sediment inventories of algal markers (chlorophyll a, PUFA) in May and August at station SK were equal to or higher than those at station GB. Because of the greater depth at station Skagerrak (270 m) and a lower primary production compared to station GB, we expected the flux of organic matter reaching the seabed to be accordingly lower. Also, earlier measurements on sedimentary ammonium fluxes and chlorophyll a at station SK did not give indications for a relatively high input of fresh organic matter (Lohse et al., 1995; Van Duyl & Kop, 1994) and the same holds for the sulphate-reduction rates measured during the expeditions of the present study (C. van der Zee, pers. comm.). Given the relatively fresh signature of the algal markers (relatively low ratio phaeopigments to chlorophyll a and a high proportion of PUFA), this implies a rapid downward transport of algal detritus. Usually, this is possible through pellet formation due to macro-zooplankton grazing (Azam et al., 1993), or increased aggregation during the senescence of diatoms (Alldredge & Gotschalk, 1989). Diatoms form an important component of the algal community in spring in the Skagerrak, while dinoflagellates or diatoms dominate in August (Karlson et al., 1996), which supports the possibility of diatom aggregation and sedimentation as a rapid transport mechanism in the Skagerrak. However, Kiørboe et al. (1990) found that an efficient microbial loop developed at the end of May in the central Skagerrak, dominated by small zooplankton and bacteria. The combination of small fecal pellets produced by the small zooplankters and the subsequent colonization and breakdown by bacteria results in low detrital sedimentation rates. Alternative to local production and sedimentation, the phytodetritus could be produced elsewhere, for example along the northern Danish coast or at the Kattegat-Skagerrak front, after which it is rapidly transported to the southern slope of the Skagerrak. Coastal Danish waters exhibit a higher production of larger phytoplankton species than central Skagerrak waters (Karlson et al., 1996), which sink faster and are less easily grazed upon. Furthermore, temporarily high nbw current velocities can develop along the southern Skagerrak slope which are capable of rapid advective transport of detrital

material (Eisma & Kalf, 1987a). If such a mechanism is important here, it should be rather efficient given the undegraded state of the sedimentary phytodetritus. Bacterial and terrestrial nature of sedimentary organic matter Bacterial (BACT) and algal (PUFA) fatty acids were significantly and positively correlated when all stations were pooled. This result agrees with that of Conte et al. (1995) who also found a significant positive correlation between these two fatty acid groups in North Atlantic sediments when the stations were considered collectively. However, in our study, by station no correlation emerges between these two markers. In other studies, a similar lack of correlation between bacterial biomass and phytodetritus in sediments was found (Jørgensen & Revsbech, 1989; Van Duyl & Kop, 1994). In our case, we attribute the overall positive correlation between bacterial and algal markers to the coincidence of high phytodetrital inventories in fine-grained sediments in combination with the well documented positive relation between grain size and bacterial biomass of sediments (Dale, 1974; DeFlaun & Mayer, 1983). Hence, a causal relationship between concentrations of BACT and PUFA is doubtful. A comparable situation is encountered concerning algal and terrestrial fatty acids: overall, a positive correlation, but no relation when stations are considered separately. Again, stations GB and SK showed elevated concentrations of these compounds in their sediments, in contrast to stations BF and FF. In the case of the German Bight, the nearby rivers Elbe and Weser are an obvious source for the terrestrial fatty acids. Terrigenous organic matter transported by rivers contains a higher concentration of long-chain fatty acids than marine organic matter (Kolattukudy, 1976; Saliot et al., 1982). Nevertheless, the dominant input of organic matter is marine, since PUFA dominate the fatty acid composition. Increased concentrations of terrestrial fatty acids were also found in near-bottom water samples from the German Bight, probably as a result of sediment resuspension (Boon & Duineveld, 1996). To some extent, this contrasts with the findings of Puls et al. (1997), who stated that the net-deposited matter in the German Bight area has a marine origin, and that fluvial particles mainly settle in the river mouth and estuary. In several studies on Skagerrak sediments, a high input of terrestrial (organic) matter has been postulated (Anton et al., 1993; De Haas, 1997; Liebezeit, 1987). We also found elevated concentrations of

Benthic supply and metabolism in the North Sea 757

long-chain fatty acids in the sediments of station SK. By contrast, the material caught with a 12-hour trap sample at 3·2 m above the bottom in February and August 1994 at station SK (Boon & Duineveld, 1996) contained very low concentrations of such fatty acids. Since the transport of suspended particles has been proposed to be pulse-like (De Haas & Van Weering, 1997), our short-term trap deployment could have missed some input of North Sea suspended matter. The most probable source of the sedimentary longchain fatty acids in the Skagerrak is the suspended matter from the North Sea. The supply of water and particles from the Norwegian and Swedish fjords and the Kattegat is only minor (Svansson, 1975), and due to the predominant eastward flow of water along the southern slope of the Skagerrak, matter from these areas is not likely to end up at our study site. Whether all the long-chain fatty acids in the Skagerrak sediments have a terrestrial origin is questionable. An accumulation of these fatty acids in sediments can, at least partly, also come from the preferential decay of short-chain fatty acids with higher degradation rates (De Baar et al., 1983; Reemtsma et al., 1990). Haddad et al. (1991) found a strong down-core increase of long-chain fatty acids in sediments from Cape Lookout Bight U.S.A., and inferred that this increase was not related to the input from terrestrial matter. Moreover, in a study by Dauwe and Middelburg (1998) the carbon isotope signal (ä13C) of the top sediment layer at this station displayed an algal signature (
22·2‰). Hence, it is likely that at least a part of these fatty acids in the Skagerrak sediments originate from the relatively high supply of refractory, marine organic matter from the North Sea (De Haas & Van Weering, 1997). Benthic detritus vs metabolism: a special case for the Skagerrak? We estimated the activity of the benthic community by using the sediment oxygen demand (SOD) and the sedimentary RNA concentrations. The RNA sampling excluded large benthos and thus its concentrations were expected to be proxies for the metabolic reaction of relatively small benthic organisms, mainly bacteria and meiofauna. Sediment oxygen demand is closely related to the presence of labile (phytodetrital) organic matter in combination with the near-bottom water (nbw) temperature (Cramer, 1990; Van Duyl & Kop, 1994; Boon et al., 1998). Hence, we expected to find an increased SOD in May, because of the spring bloom sedimentation of labile detritus and increased water temperatures. This was indeed the case at all stations.

T 3. Carbon fluxes (mg C m
2 day
1) calculated from chlorophyll a trap flux, chlorophyll a inventory and SOD at station Skagerrak

February May August

Trapa

Inventoryb

SOD

0·21 no data 0·30

63 1110 267

43 146 71

c

a

Using a C:Chla ratio of 50; trap data from Boon and Duineveld (1996). b Using the formula ‘ Flux=exponential degradation rate (0·03 day
1)*chlorophyll a inventory ’ (Sun et al., 1993), and a C;Chla ratio of 50. c Using an oxygen to carbon conversion of 77% (the other 23% is used for nitrification, see Canfield et al. 1993).

As a result of even higher near-bottom water temperatures in August, a further increase of the SOD was noted at Station GB. This phenomenon is possible through a build up of labile organic matter in sediments due to the spring bloom sedimentation and its subsequent degradation during summer and autumn (Roden & Tuttle, 1996; Boon & Duineveld, 1998). However, while the nbw temperature at station FF increased c. 6 C from May to August, and no decrease was found in the chlorophyll a and fatty acid inventories, the SOD showed a 50% drop in the latter month. Earlier studies by Cramer (1990) and Boon et al. (1998) did show a conjointly maximum SOD and nbw temperature in August at this station. Station GB did show this relation, with maximum temperatures and SOD co-occurring in August. This station is known to demonstrate the highest nutrient and oxygen fluxes measured in the North Sea (Lohse et al., 1995), as well as the only area in the North Sea with a predominance of sulphate-reduction in total carbon mineralization (Upton et al., 1993). A quite unexpected situation was observed at station SK. The Skagerrak sediments had a maximum SOD in May, with a decrease in August, co-varying with the concentration of labile organic matter. Interestingly, when comparing inventories of labile organic matter and SOD at stations GB and SK, we consistently found much lower SOD values at station SK, while concentrations of labile organic matter were comparably high. Our SOD values at station SK agree with earlier studies (Van Duyl & Kop, 1994; Lohse et al., 1995), as well as with the relatively low nutrient fluxes and sulphate-reduction rates at this station, measured during the cruises of this study (C. van der Zee, pers. comm.), which all indicated a relatively low sediment metabolism. In Table 3, the relevant data on chlorophyll a trap fluxes, chlorophyll a inventory and SOD are summarized for station SK. For comparison,

758 A. R. Boon et al. 0.50 0.45

Ratio RNA:SOD

0.40 0.35 0.30 0.25 0.20 0.15 0.10

SK Aug

SK May

SK Feb

GB Aug

GB May

GB Feb

FF Aug

FF May

FF Feb

BF Aug

BF May

0

BF Feb

0.05

Station, Month

F 8. Ratio of RNA inventory to sediment oxygen demand.

they are expressed in carbon units (for explanation see legend). It is clear that carbon flux to the sediment (from inventory) and sediment carbon mineralization (from SOD) show a large mismatch. At the other stations this discrepancy is much smaller. A study on North Sea sedimentary amino acids by Dauwe et al. (1999) also showed a relatively high concentration of enzymatically available amino acids at station Skagerrak. An earlier study (Boon & Duineveld, 1998) showed a good agreement between these two variables on an annual scale at stations in the southern North Sea. In addition to the carbon discrepancy at station SK, the trap flux of chlorophyll a at this station is insufficient to sustain the carbon fluxes derived from both the chlorophyll a inventory and the SOD. Questionable is the use of the carbon to chlorophyll a ratio of 50 (from Boon & Duineveld, 1998) for calculating the labile carbon trap flux. From data on phaeopigment to chlorophyll a ratios and in situ nearbottom water C:Chla ratios (up to >1000, Boon & Duineveld, 1996) it can be expected that this ratio might be higher. However, when assuming this, the supply of carbon to the sediments as calculated from the chlorophyll a inventory would be proportionally higher, resulting in a comparable gap between trap carbon flux and inventory carbon flux, and in an even larger gap between the carbon flux derived from the inventory and that from the SOD. Further, the exponential degradation rate used to calculate the carbon flux from the chlorophyll a, could be somewhat lower due to the relatively low near-bottom water temperature at station SK. Sun et al. (1993) measured a decay rate of 0·02 day
1 for chlorophyll a at a temperature

of c. 10 C. However, this would not explain the above mentioned discrepancies. The daily carbon fluxes from Table 3 can be converted to the annual supply of carbon to the Skagerrak sediments. To this end, we assume that the data give a representative estimate for the minimum (Feb), maximum (May) and intermediate (Aug) input, equally divided over the three periods they represent (respectively winter, spring/early summer and late summer/autumn). The yearly carbon supply thus amounts to 175 g C m
2 yr
1, which is close to the estimated local primary production of 100 to 150 g C m
2 yr
1 (Skogen et al., 1995). This figure is too high because it is unlikely that the complete primary production sediments to the sea-floor. The other metabolic parameter, the sedimentary RNA concentration, also showed an anomalous situation for the Skagerrak station. Although the RNA inventory was closely correlated to the SOD values, there are large spatial differences in RNA to SOD ratio (Figure 8). Especially at station SK this ratio is increased. While such a high ratio could originate from anaerobic metabolism, other studies showed that sulphate reduction and denitrification are relatively low in these sediments (C. van der Zee, pers. comm.; Lohse et al., 1995). The correlation between RNA and both the chlorophyll a and PUFA inventories is highly significant (R2 =0·96 respectively 0·90, P<0·001). This close correlation between proxies of algal matter and RNA on the one hand and the discrepancy between the (mainly bacterial) SOD and RNA on the other hand, possibly indicates that the RNA is derived from algae and does not originate

Benthic supply and metabolism in the North Sea 759

from sediment bacteria. This would imply that not only DNA, but also sedimentary RNA is partly detrital, which is contradictory to the common notion that RNA is quickly lost from dying cells. Although faunal components may have contributed to the sedimentary RNA pool, there is no reason to expect this to be more important at station SK than at the other stations (Dauwe et al., 1998). Clearly, the source of the sediment nucleic acids needs further investigation. Apparently, neither the water temperature nor a larger carbon to chlorophyll a ratio can provide an answer to the large mismatch between the supply of labile organic matter and sediment metabolism at station SK. Furthermore, there is no oxygen limitation in the near-bottom water (Table 2) which could suppress aerobic metabolism and chemical oxidation. It is hypothesized that two possible—not mutually excluding—mechanisms are responsible for the relatively high concentrations of labile organic matter in Skagerrak sediments. The first is a mechanism earlier proposed by Keil et al. (1994). They showed a slowing of mineralization of labile organic matter up to five orders of magnitude due to sorption of these compounds in sediments with a high mineral surface area. In an electron-microscopy study of suspended material and sediment, Ransom et al. (1997) showed that labile organic matter in fine-grained sediment exists as ‘ blebs ’, mainly associated with clay minerals. They suggested that low permeability is responsible for the depressed degradation rates and the enhanced organic matter preservation in finegrained sediments. Since the Skagerrak sediments contain 50% silts and about 20% clayey particles, this mechanism could well apply here. The other proposed mechanism to explain the relatively high concentrations of sedimentary labile compounds at station SK is the earlier mentioned down-slope advection of labile organic matter from the shallower coastal waters of northern Denmark. Periodically, strong currents occur in the southern part of the Skagerrak (Eisma & Kalf, 1987a; De Haas & Van Weering, 1997) which could lead to strong down-slope transport of algal detritus from these waters to deeper sediments. Following pulses of strong water currents could then remove the labile organic matter again, leaving enough material to sustain the SOD found in this study. Clearly, our study gives support to the occurrence of interesting sedimentation and/or geochemical phenomena occurring in the Skagerrak benthic environment. Further studies are needed to resolve these processes, which are a major issue for carbon transport, cycling and diagenesis at fine-grained clayey shelf slopes.

Acknowledgements The authors thank the crew of the RV Pelagia for their on-board work during the 1994 sampling surveys. We are grateful for the suggestions, made by three anonymous reviewers, which helped us improve the manuscript. Financial support for this research has been provided by the Netherlands Organisation for the Advancement of Science (NWO), project VvA, under grant 770-18-235.

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