Pergamon Diffusive and total oxygen uptake of deep ... - Science Direct

Pergamon

Deep-SeaResearch1, Vol.41, No. 11/12,pp. 1767-1788,1994 Copyright© 1994ElsevierScienceLtd Printedin GreatBritain.All tightsreserved 0967-0637,94$7.00+ 0.00

0967--0637(94)000211--4

D i f f u s i v e a n d total o x y g e n u p t a k e o f d e e p - s e a s e d i m e n t s in the e a s t e r n S o u t h A t l a n t i c O c e a n : in situ a n d l a b o r a t o r y measurements RONNIE NOHR G L U D , * t JENS K . GUNDERSEN,*t B o BARKER JORGENSEN,t NIELS PETER REVSBECH* a n d HORST D . SCHULZ~

(Received 24 June 1993; in revised form 20 December 1993; accepted 13 April 1994)

Abstract--Total 0 2 uptake rates were measured by the benthic flux chamber lander ELINOR, and 0 2 microprofiles were measured by the profiling lander PROFILUR in the eastern South Atlantic. Diffusive 0 2 fluxes through the diffusive boundary layer and the depth distribution of 02 consumption rates within the sediment were calculated from the obtained microprofiles. The depth integrated 0 2 consumption rate agreed closely with the diffusive 02 uptake at all stations. Total 02 uptake was 1.2-4.2 times the diffusive 0 2 uptake, and the difference correlated with the abundance of macrofauna in the sediment. Diffusive 02 uptake and 02-penetration depths correlated with the organic content of the sediments and exhibited an inverse correlation with water depth. Total and diffusive rates of in situ 02 uptake were higher than previously published data for shelf and abyssal sediments in the Atlantic, but were comparable to rates from upwelling areas in the eastern Pacific. Laboratory measurements on recovered sediment cores showed lower 02 penetration depths and higher diffusive uptake rates than in situ measurements. The differences increased with increasing water depth. We primarily ascribe this compression of 02 profiles to a transiently increased temperature during recovery and enhanced microbial activity in decompressed sediment cores. Total 02 uptake rates measured in the laboratory on macrofauna-rich stations were, in contrast, lower than those measured in situ because of underrepresentation and disturbance of the macrofauna.

INTRODUCTION

THE 02 uptake of sediments has been widely used as a measure of the total rate of mineralization and community metabolism. One common technique for measuring the 02 uptake of sediments has been to enclose an area of sediment and measure the change in 09 concentration of the overlying water. This technique gives the total 02 uptake of the sediment. Both laboratory-incubated sediment cores and in situ benthic flux chambers have been used (e.g. PAMATMAT,1971; SMITH,1979; JAHNKEand CHRISTENSEN, 1989; HALL et al., 1989). In recent years, microelectrode measurements of 02 concentration profiles above and in the sediment have been used to calculate the diffusive oxygen uptake of sediments and respiration in the oxic surface zone (REVSBECH and JORGENSEN, 1986; REIMERS et al., 1986; RASMUSSENand JORGENSEN,1992). The O2 respiration of benthic *Institute of Biological Sciences, Department of Microbial Ecology, University of Aarhus, Ny Munkegade, DK-8000 Aarhus C, Denmark. tMax Planck Institute for Marine Microbiology, Fahrenheitstrasse 1, 28359 Bremen, Germany. ~:Fachbereich Geowissenschaften der Universit/it Bremen, 28334 Bremen, Germany. 1767

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al.

fauna and transport of oxic water into their burrows have been quantified by measuring the respiration rate and ventilation activity of individual animals or by subtracting the diffusive from the total O2 uptake (ALLER, 1978; KRISTENSEN,1985; KANNEWORFand CHRISTENSEN, 1986; GgAE et al., 1982; RASMUSSEN and JaRGENSEN, 1992; ARCHER and DEVOL, 1992). Oxygen is energetically the most favourable electron acceptor available in nature and is the first to be depleted below the sediment surface. In shelf sediments with a high respiratory activity,O2 penetrates only a few mm, whereas in sediments with a low organic input the penetration depth may increase to many cm or dm (GUNDERSENand JORGENSEN, 1991; REIMERS, 1987). Immediately above the sediment surface a 0.2-1.2 mm thick diffusive boundary layer (DBL) has been demonstrated, which may influence the rate of 02 uptake (J~R6ENSEN and REVSBECH, 1985; ARCHER et al., 1989; JOR6ENSEN and DES MAgalS, 1990; GUNDERSEN and JORGENSEN, 1990). Just like other dissolved species, 02 moves through the D B L by molecular diffusion along a linear concentration gradient from which the diffusive 02 uptake can be calculated. Diffusion also controls 02 transport through the thin oxic surface zone of impermeable sediments, but here the 02 concentration decreases with depth due to concurrent consumption of 02 (CRANK, 1983). The depth distribution of aerobic respiration in the oxic zone can be calculated from the curvature of the profile (CRANK, 1983; N~ELSEN et al., 1990). The benthic fauna drives a convective transport of oxic water deep into the sediment and, by burrowing, mixes the sediment and creates microzones with a complex three-dimensional structure (GRUNDMANIS and MURRAY, 1977; ALLER and YINGST, 1985). In the present study we compared measurements of total 0 2 uptake with two methods for studying the diffusive oxygen consumption in the sediment: flux calculations from concentration gradients in the D B L and modelling of aerobic respiration in the oxic sediment zone. In situ measurements were compared to measurements carried out in a shipboard laboratory on sediment cores from water depths of 400-5000 m.

MATERIALS AND METHODS Study area

Laboratory measurements of total and diffusive 02 uptake were carried out at 13 stations, in situ measurements of 02 profiles were conducted at eight stations, and in situ total 02 uptake was measured at six stations during a cruise of R.V. Meteor in the South-East Atlantic during the period 27 December 1991 to 3 February 1992. The locations of the sediment stations are presented in Table 1 and Fig. 1. The stations GeoB1701, GeoB1702 and GeoB1703 were located in the river cones of the rivers Niger, Congo and Cunene, respectively. The other stations were located on three transects west of Namibia in the Benguela upwelling area. In the following, stations are referred to only by their number (see Table 1).

Laboratory measurements

At each station measurements in the laboratory were carried out on two 25-45 cm long sediment cores (I.D. 62 mm) which had been recovered by a multiple corer (BARNETet al., 1984). The sediment surface appeared to be undisturbed, as microtopography created by newly settled aggregates and macrofauna could be observed, and the overlying water was

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Oxygen uptake of deep-sea sediments

clear. Immediately after recovery, the 0 2 concentration in the overlying water was determined by Winkler titration (SxRICKLANDand PARSON, 1972). The 02 concentrations measured in this way agreed within + 5% with CTD measurements 50 m above the sea floor. Within 20 min after recovery, the uncapped sediment cores were submerged in an incubation tank with sea water maintained at in situ temperature and continuously flushed with an air/N 2 gas mixture to maintain in situ 02 concentration. The overlying water in each core was stirred by a small Teflon-coated magnet driven by a rotating external magnet. The stirring resulted in an average D B L thickness similar to what was observed in situ. To ensure that the oxygen profile was in a steady state, the two cores were preincubated in the tank for at least 3 h before measurements. Total and diffusive 02 uptake were measured by Clark type O2 microelectrodes with a guard cathode (REVSBECH, 1989a). The outside diameter of the microelectrode tips was 520~m, and the shaft diameter, 10 mm from the tip, was about 250/~m. The microelectrodes had stirring effects (i.e. the signal increase in flowing vs stagnant water) of < 1 % , and a 90% response time of 85% of the in situ value. The diffusive O2 uptake, the 0 2 penetration depth, and the O2 consumption rates in discrete layers of the sediment were calculated from the 02 microprofiles. The position of

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the sediment surface could be determined from the microprofiles as a change in slope of the oxygen concentration gradient due to impeded diffusion (REvSBECn, 1989b; SWEERXS etal., 1989). The 02 penetration depth could generally be determined directly from the 02 profiles as the depth where the signal of the O2 microelectrode reached a constant, low reading (i.e. the zero current). However, when the oxygen penetration exceeded more than 35 mm in foraminifera-rich sediments, it was impossible to measure a complete profile before the microelectrodes broke, and the 02 penetration depth was then estimated by linear extrapolation of the last part of the measured profile. The estimated penetration depths therefore represent minimum values. The diffusive 02 uptake (J) in situ and in the laboratory was calculated from 02 microprofiles by Fick's first law of diffusion (1) and the linear concentration gradient measured in the DBL (CRANK, 1983; RASMUSSEN and JORGENSEN, 1992). This allows a calculation of the diffusive 02 uptake without an (often uncertain) estimate of the diffusive characteristics within the sediment ]

=

-

D dC(z) , dz

(1)

where D is the diffusion coefficient of 02 in sea water, and C(z) is the concentration of 02 at depth z. Values of D were taken from BROECKERand PENG (1974) and were recalculated to in situ temperature by the Stokes-Einstein relation (LI and GREGORY, 1974). Provided that the sediment has a uniform porosity and the 02 consumption has zero order kinetics, the distribution of 02 consumption rate per unit volume can be modelled by curve-fitting as described by NIELSENet al. (1990). The effective diffusive coefficient of the sediments (Ds) was calculated from Ds = D ~)m-1 (ULLMAN and ALLER, 1982) with a porosity (q~) of 0.95 and m value of 3. The 02 consumption in discrete layers was determined per unit area by multiplying by the thickness of the layer. The sum of the modelled 02 consumptions in each layer gave the depth-integrated O2 consumption, which theoretically should equal the diffusive 02 consumption (RASMUSSEN and JORGENSEN, 1992).

RESULTS A series of 0 2 profiles obtained by the PROFILUR at five stations with water depths ranging from 600 to 4986 m are shown in Fig. 2. The 02 penetration depth increased with increasing water depth. The shallow 02 penetration at Sta. 1713 was partly due to the low O2 concentration in the overlying water. At Sta. 1723 (Fig. 2E), the microelectrodes broke before reaching the anoxic layer, which obviously was situated much deeper than at the other stations, and the 02 penetration depth could therefore only be estimated, thus preventing modelling of the oxygen consumption rate. The 02 concentration in the bottom water was uniformly high at the deeper stations but decreased gradually with decreasing water depth (Table 2). The CTD~profiles measured over the continental slope showed that the oxygen minimum was situated at 300--400 m depth. The lowest 02 concentration was accordingly obtained at Sta. 1704 at a water depth of 399 m. The calculated oxygen respiration rates (Fig. 2) generally were relatively higher at the sediment surface and at oxic-anoxic interface. The depth-integrated 02 consumptions were not significantly different from the diffusive oxygen uptake calculated from the gradients in DBL (Table 2).

1773

Oxygen uptake of deep-sea sediments Oxygen respiration (nmol cm'3day q) 500 1000

0

Oxygen respiration (nmol cm-°day 1) 500 1000 1500 0

1500 0

Oxygen respiration (nmol c m ° d a y "t) 500 1000 1500

10

2o 0

3O A 4C

o

Sta. 1713 w.d. 600 m

5b 16o l~o 2bo25oo Oxygen (ttM)

Sta. 1703 w.d. 1743 m

B

Sta. 1711 w.d. 1960 m

50 100 150 200 250 0 Oxygen (p,M)

Oxygen respiration (nmoi c m ° d a y -t) 50 100

50 100 150 200 250 Oxygen (p,M)

Oxygen respiration (nmol cm'°day "l) 50~ 100

150

0

/

150

10 -

1 3o

Sta. 1723

w.d. 4986 m C 400

w.d. 3100 m 50 100 150 200 250 0 Oxygen (ItM)

D

/

/

50 100 150 200 250 Oxygen (ttM)

Fig. 2. In situ 0 2 microprofiles measured with a spatial resolution of 0.1 mm at five different water depths. The calculation 02 consumption rates in discrete layers are shown (notice the different scale in (A) and (B) compared to (C), (D) and (E); w.d. = water depth).

A detail of an O2 profile at the sediment-water interface from Sta. 1719 (Fig. 3) illustrates the linear 02 concentration gradient in the DBL from which the diffusive 02 uptake is calculated and the change in slope of the 02 gradient at the sediment surface. The DBL thickness estimated as described by JORGENSENand REVSBECH(1985) was 580/~m. The average thickness of the DBL at the different stations varied between 340 and 850 ktm (Table 2). Figure 4 shows that the diffusive 02 uptake exhibited a roughly linear decrease, and the 02 penetration depth appeared to follow an exponential increase, with increasing water depth. Several parameters which are expected to affect the diffusive 02 uptake and the 02

K. N.

1774

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1775


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150

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Oxygen (pM) Fig. 3. Detail of an O2 microprofile from Sta. 1719. The sediment surface and upper boundary of the diffusive boundary layer (DBL) are indicated by the line at depth zero and the broken line, respectively.

5 A

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Water depth (km)

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Water depth (km)

Fig. 4. Diffusive oxygen uptake (A) and oxygen penetration depth (B) in relation to water depth. Linear regression analysis (A) yielded a correlation coefficient, r2, of 0.61. The broken line is hand drawn. Standard deviations are shown.

penetration depth also change with water depth, and many of them are interdependent (SMITH and HINGA, 1983). The organic content of the sediment was, however, the single parameter that correlated best with our data (Fig. 5). The linear correlation coefficient (r 2) between the organic content of the uppermost 0-1 cm of the sediment and the diffusive 02 uptake was 0.77. According to Fig. 5B, the 02 penetration depth approached zero at high organic content, and the 02 penetration increased dramatically when the organic content

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R . N . GLut) et al.

200

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Fig. 5. The diffusive oxygen uptake (A) and the oxygen penetration depth (B) plotted against the organic content of the top 0-1 cm of the sediment (data supplied by P. J. M/.iller). The broken line is hand drawn. Standard deviations are shown.

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Oxygen (pM) Fig. 6.

An in situ 02 profile from Sta. 1702 at 3107 m water depth. The microelectrode had penetrated an animal burrow below 80 mm d e p t h

was very low. It should be kept in mind that the O2 penetration depths of 200 m m and 55 m m were estimated from extrapolation and therefore represent minimum values. The 0 2 profile shown in Fig. 6 was obtained at Sta. 1702 at 3107 m water depth. A peak of oxygen appeared at a depth of about 85 m m in the otherwise anoxic layer, and was probably due to a ventilated tube of a burrowing animal. The 02 concentration in the burrow almost reached bottom-water values, which is possible only if there was active


1777

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Time (h) Fig. 7. A calibrated recording by the 02 electrodes placed in the lid of the benthic flux chamber lander ELINOR during a deployment at 3107 m water depth. (A) Data obtained during sinking through the water column; (B) measurements during the incubation. 1, ELINOR landed; 2, lid is closed; 3, scoop is closed; 4, ballast is released. p u m p i n g of o x y g e n a t e d water t h r o u g h the b u r r o w or a flushing resulting f r o m a pressure gradient b e t w e e n the two openings of the b u r r o w , the so-called "Bernoulli effect" (VOGEL, 1981). A typical r e a d - o u t from o n e of the microelectrodes during a d e p l o y m e n t of E L I N O R is shown in Fig. 7. T h e 0 2 c o n c e n t r a t i o n d o w n t h r o u g h the water c o l u m n was m e a s u r e d by the microelectrode until E L I N O R landed 1.3 h after the start of the d e p l o y m e n t . A f t e r 11 min of sinking the 0 2 m i n i m u m zone was obvious at 385 m depth (panel A). T h e 02 c o n c e n t r a t i o n then increased to a m a x i m u m value at 2100 m, after which it slowly levelled off to the b o t t o m water value. A f t e r the instrument settled o n the sea floor the signal was constant until the lid d o s e d , and then decreased linearly during the incubation (panel B). T h e total 0 2 u p t a k e was calculated f r o m the slope o f the line, which was 0.69 ~ M h - l , and

1778

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GLUD

et al.

from the water height inside the chamber. The quantitative effect of the fauna on the oxygen uptake of the sediment was obtained by comparing the diffusive 02 uptake to data obtained by ELINOR. The total 02 uptake measured in situ was larger than the diffusive Oz uptake at all stations (Table 2), but the ratio between the two rates of 02 uptake varied. At Sta. 1719 the ratio was 4.2, but it was only 1.2 at Sta. 1702, where there was no macrofauna in the sediment. The largest difference between total and diffusive 02 uptake (10.7 mmol m -2 day -~" a factor of 3.2) was observed at Sta. 1703 at 1747 m water depth, where the sediment was densely populated by the agglutinating foraminiferan Rhabdammina abyss o r u m (CARPENTER,1869) (Table 3), which has shells up to 20 mm long and 5 mm wide. The total 02 uptake did not correlate as well with water depth or organic content of the sediment as did the diffusive 02 uptake. There was, however, a strong correlation between the total 02 uptake and the dry weight of macrofauna in the sediment (Fig. 8A). A linear regression of the data points gave a correlation coefficient (r 21 of 0.87, but a curve fit the six data points better. The difference between the total and diffusive 02 uptake also correlated well with the amount of macrofauna in the sediment (Fig. 8B), and the total 02 uptake was close to the value for diffusive 02 uptake when macrofauna was absent. Generally the 02 penetration depth was smaller when measured in the laboratory. Further, both the diffusive O 2 uptake and depth-integrated 02 consumption values obtained from profiles measured in the laboratory gave higher values than those calculated from in situ data. An example of the difference between data obtained in situ and in the laboratory is shown in Fig. 9. The 0 2 penetration depth decreased from 35.0 mm when measured in situ to 24.5 mm when measured in the recovered sediment core, while the corresponding diffusive 02 uptakes increased by 70% from 1.4 to 2.3 mmol m --2 day-i The modelled depth-integrated 02 consumption increased equally (Fig. 9). The ratio between the diffusive 02 uptake measured in the laboratory and that measured in situ increased linearly with increasing water depth (Fig. 10A). At 600 m water depth the diffusive 02 uptakes measured in the laboratory and in situ were almost Table 3.

Dry weight of macrofauna (including burrow linings)

Macrofauna

Macrofauna

Sta.

in E L I N O R (g m -2)

sediment cores ( g m 2)

in Dominant

I701

--

11.00

--

1702

0.00

0.00

--

1703

101.50

61.44

Foraminifera

1704 1708

---

20.25 O. O0

Bivalvia --

1711

3.75

1712

--

1713

36.72

1719

33.01

0.00 0.58

Polychaeta

4.88

Polychaeta

1.56

Polychaeta

1720

--

tl.76

Polychaeta

1721

7.97

7.31

Foraminifera,

1722

--

2.85

Bivalvia

1723

--

0.00

--

-- No data.

taxa

Polychaeta

1779


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20 A

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Dry weight of macrofauna (g m-2)

100

Dry weight of macrofauna (g m-2)

Fig. 8. (A) The total O 2 uptake in situ and (B) the difference between total and diffusive 02 uptake in situ plotted against the dry weight of macrofauna in sediment recovered by ELINOR. The full line shows the linear regression while broken lines are hand drawn.

Oxygen respiration (nmol cm-3 d-l) 0

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0

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Oxygen concentration {~M)

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250

Oxygen concentration (l.tM)

Fig. 9. Two 0 2 microprofiles obtained in the laboratory and in situ, respectively, at Sta. 1702. The spatial resolution is 0.1 mm. The diffusive O 2 uptake was calculated to be 2.51 and 1.37 mmol m -2 day-l, and the O 2 penetration depths were 24.5 and 35.0 mm, respectively.

1780

R.N. GLUDet al. 1.2 A

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Fig. 10. (A) The ratio between the diffusiveO2 uptake measured in the laboratory and in situ and (B) the ratio between the O2 penetration depth measured in the laboratory and in situ plotted against water depth. Standard deviations are shown. identical, but at 4986 m the diffusive 0 2 uptake measured in the laboratory was 3.5 times higher than that measured in situ. Profiles obtained at the two stations with high carbonate sediments at about 3000 m depth showed smaller differences than those at the other stations. A similar trend was seen with the 02 penetration depth. At 4986 m depth the 02 penetration measured in the laboratory was only 25% of that estimated from in situ profiles, whereas no difference was seen at 0.6 km (Fig. 10B). The total 02 uptake measured in the laboratory also differed from the rate measured in situ (Table 2). At the stations with high densities of macrofauna (Table 3), the total 02 uptake rates measured in the laboratory were lower than in situ rates, but at stations with small amounts of macrofauna (Table 3) and large water depth the rates measured in the laboratory were higher than those measured in situ, as was the case with the diffusive 02 uptake. DISCUSSION Data obtained f r o m in situ microprofiles

The modelled depth-integrated 0 2 consumption generally agreed well with the diffusive 02 uptake calculated from the 02 gradient in the D B L (Table 2), as was also reported from a study in coastal waters (RASMUSSEN and JORGENSEN, 1992). The depth distribution of 02 consumption mostly showed three zones, with relatively high 0 2 consumption rates at the upper and lower parts of the oxic zone as seen in Fig. 2C and D. The higher 02 consumption near the surface was probably due to a higher concentration of easily degradable organic material, whereas the higher 02 consumption near the oxic-anoxic interface probably reflects the oxidation of reduced organic and inorganic compounds from the anaerobic mineralization in deeper layers (GuNDERSEN and JORGENSEN, 1991). The relatively low activity in the middle of the oxic zone thus probably reflects a limitation of electron donors. The relative contribution of 02 consumption at the oxic-anoxic interface decreased with increasing water depth (data not shown), consistent with the fact

Oxygenuptake of deep-seasediments

1781

that at greater depths the total mineralization of organic material becomes increasingly dominated by aerobic oxidation (JAHNKE et al., 1989; CANFIELD,1992). At Sta. 1703, at 1747 m water depth, no increase in the O2 consumption rate at the oxic-anoxic interface could be observed, but a relatively high O2 consumption was apparent just at the sediment surface. Such a profile may reflect a recent sedimentation episode with an input of easily degradable organic matter to the sediment surface. A continuous upward diffusion of reduced compounds from the anoxic sediment layer may later reestablish a reoxidation zone at the bottom of the O2 profile. The sediment at Sta. 1703 accordingly had the second-highest concentration of organic matter of all those analyzed (P. MULLER, unpublished results). The O2 profiles obtained at 4986 m water depth (Fig. 2E, Sta. 1723) showed a relatively sharp decline in the top 5 mm of the sediment, below which the O2 concentration decreased only slowly with depth until the microelectrode broke at 35 mm depth. Such a profile is caused by a relatively high 02 consumption rate near the sediment surface, below which the mineralization rate is very low. Other researchers have also reported deep linear 0 2 gradients in the eastern Atlantic (WILSONe t al., 1985; JAHNKEet al., 1989). The depth-integrated 0 2 consumption was modelled from the O2-microprofiles and an assumed constant average porosity of 0.95 in the oxic zone. Published porosity profiles from deep sea sediments generally show a relative sharp decline from 1 at the surface to 0.95-0.80 at a depth of 10-15 mm, where it becomes fairly constant (ARCHERet al., 1989; JAHNKE et al., 1986). It there were similar decreases in porosity at our stations, then we have underestimated the 02 consumption rates near the sediment surface and overestimated the rates in the lower part of the profiles. Generally calculations using porosity profiles as outlined above showed the same depth distribution of the consumption rates as when a constant porosity profile was used. Using a lower porosity like 0.90 instead of 0.95 would decrease the depth integrated 02 consumption rate calculated, but not to an extent where it would be significantly different from the diffusive oxygen uptake. The thickness of the DBL in situ generally increased with increasing water depth (Table 2). However, the thickness of the DBL is determined by parameters such as water flow velocity, temperature, pressure and sediment roughness (BoUDREAUand GUINASSO,1982) and not directly by water depth. Recent laboratory studies have shown that, because of a three-dimensional perturbation of the flow field around microelectrodes, the thickness of the DBL is underestimated by 25-45% when measured from O2-microprofiles (GLuD et al., 1994). The true thickness of the DBL should therefore be correspondingly larger. Compression of the DBL will, however, not have any significant effect on the 0 2 gradient in the DBL, because of the low activity and deep O2 penetration depth. This also implies that if stirring rates inside the chamber of ELINOR during the measurements created a DBL thickness slightly different from the in situ value, the effects on the obtained total 02 uptake would be negligible. Measurements of total

0 2

uptake and the effect of fauna

In coastal waters it is well documented that infaunas have an important role for the mineralization of organic material and the exchange of solutes across the sediment-water interface (ALLER, 1988; KRISTENSEN, 1988; RASMUSSEN and JORGENSEN, 1992). The infauna increases the O2 uptake of sediments partly by creating secondary oxic surfaces within the sediment (e.g. burrow walls) and partly by their own respiration. In continental

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slope sediments the effect of fauna on the exchange rate of oxygen has been assumed to be of minor importance, and the effect is believed to be negligible in abyssal sediments (SMITH and HINGA, 1983; REIMERS and SMIXH, 1986; REIMERSet al., 1986; JAHNKEet al., 1990; ARCHER and DEVOL, 1992). However, plutonium and microtektite profiles in deep-sea sediments have revealed a significant vertical mixing of sediment particles which was ascribed to burrowing infauna, even over short time scales of 10 years (NosHKIN and BOWEN, 1973; StuNK and GUINASSO,1977; GUINASSOand SCmNK, 1975). Profiles of 21°Pb and 32Si have also shown that the intensity of deep-sea sediment mixing can be very patchy, implying a high spatial variation in faunal activity (DEMASTERand COCHRAN,1982). The patchiness of infauna abundance was confirmed by replicate box cores obtained from the central North Pacific by HESSLERand JUMARS(1974), who observed very different density and diversity of fauna within a relatively small area. The finding of vertical open Trichichnus burrows down to more than 2 m depth in sediments at 5000-6000 m depth in the eastern North Atlantic also suggests that benthos can play an important role in the benthic mineralization processes in some deep-sea sediments (WEAVERand SCHULTHEISS, 1983). The steep 02 gradients around the burrow shown in Fig. 6 indicate an intense oxygen consumption in the surrounding sediments. A minimum estimate of the oxygen respiration in the sediment surrounding the burrow was calculated by assuming radial diffusion and a burrow diameter of 6 mm and also by assuming that the microelectrode went through the centre of a cylindrical burrow and then perpendicularly into the burrow wall. The value obtained was nine times higher than the respiration rate calculated for the sediment surface with a porosity of 0.95 at both depths. Assumption of a porosity of 0.80 in the surroundings of the burrow resulted in a six-fold higher 02 consumption rate around the burrow compared to the surfaces. These estimates imply that the local 02 uptake can be significantly enhanced by fauna inhabiting the sediment. The in situ data presented here show significant differences between total and diffusive 02 uptake at all but one station (1702), and the difference is correlated with the abundance of fauna inhabiting the sediment (Fig. 8B). At Sta. 1702, where no macrofauna was observed in the sediment, there was no significant difference between diffusive and total O2 uptake measured in situ. The abundance of fauna measured in the chamber of ELINOR was highest at the three shallowest stations (1703, 1713, 1719). At 1747 m water depth (Sta. 1703) the abundance especially of benthic foraminifera increased the total O~ uptake by more than a factor of three over the diffusive 02 uptake. Even at 3095 m depth (Sta. 1721) the presence of macrofauna (dominated by polychaeta and foraminifera) doubled the rate of 02 uptake by the sediment (Table 2). It is important to notice that the faunas inhabiting the sediments at the different stations were very different. The station with the highest dry weight of macrofauna was dominated by benthic foraminifera, and a major part of the weight of this animal is the biologically inactive shall. This explains the relatively low total O2 uptake for this station despite the large dry weight of infauna. The one-dimensional diffusion model (1) used to calculate the diffusive 02 uptake from the microprofiles assumes a smooth surface of the sediment and the upper boundary of the DBL (CRANK, 1983). Because of sediment topography, however, the total 02 uptake tends to be larger than the diffusive O2 uptake, even without fauna present (JORGENSENand DES MARAIS, 1990; GUNDERSEN and JORGENSEN, 1990). The difference between the diffusive and the total 02 uptake due to this effect is dependent on the roughness of the sediment surface, the thickness of the DBL, and the 02 penetration depth (JORGENSENand DES

Oxygenuptake of deep-seasediments

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MARAIS,1990). Measurements conducted on sediment cores in which no macrofauna was observed, showed that the total O2 uptake was always higher than the diffusive 02 uptake (Tables 2 and 3). Because of the relatively smooth microtopography of the sediments and the generally deep O2 penetration, the differences were small, however, and were in most cases within the limits of uncertainty. Recent studies have shown that central stirring in respiration chambers creates pressure gradients that can result in advective pore water transport through permeable sediments or enhance flow through burrows (HOTrEL and GUST, 1992). Such effects can enhance the exchange rate over the sediment-water interface by up to six-fold in sandy sediments (HOTrEL and GUST, 1992). However, since the total and the diffusive 02 uptake differed only insignificantly at Sta. 1702, which had the most coarse grained and calcareous sediment, the stirring pressure effects inside the respiration chamber of ELINOR were apparently of minor importance for the measured exchange rates. High rates o f 0 2 uptake in the eastern South Atlantic

The benthic 02 uptake rates presented here, and especially the total 02 uptake rates, are generally higher than published data for shelf and abyssal sediments in the Atlantic (SMITH, 1978; PATCHINGet al., 1986; JAHNKEet al., 1989). Theoretical rates of total benthic 02 uptake at the stations could be calculated from the predictive equations for benthic 02 consumption in the Atlantic Ocean proposed by SMITH and HINGA (1983) and from regional primary production data accumulated by BERGERet al. (1987). The calculated rates were from 4 (Sta. 1721) to 8 (Sta. 1723) times lower than our in situ measurements of the diffusive Oz uptake. In previous studies in the eastern North Atlantic, measured 02 uptake rates were up to 9 times higher than estimates made from the same predictive equations (PATCHINGet al., 1986). Predictive equations for the coastal Pacific upwelling margins made by JAHNKEand JACKSON(1987) fit our in situ diffusive 0 2 uptake data much better, even though they are still a factor of 2 higher at the shallow stations. Generally, our diffusive Oa uptake measurements are comparable to rates measured in the eastern upwelling regions of the Pacific (SMITHet al., 1983; REIMERSand SMITH, 1986; SMITH, 1987; JAHNKEet al., 1990; ARCHERand DEVOL,1992). The measured total O2 uptake in an area with a patchy distribution of fauna will be very dependent upon the placement of the respiration chamber. Our in situ total 02 uptake rates at the most shallow stations (Stas 1713 and 1719) are significantly higher than previously reported from comparable water depths, probably due to large densities of fauna at the investigated spots. Station 1703 has exceptionally high rates of total 02 uptake both in situ and in the laboratory measurements, which corresponded to very high densities of benthic agglutinating foraminifera, suggesting a high input of organic material. The fact that the 02 uptake rates correlated better with the organic content of the sediment than with the water depth is probably due to the upwelling areas in the study region, which have large local variations in pelagic primary production and sedimentation. Further, lateral and down-slope input of organic material can be important in continental margin areas (THORPE and WHITE, 1988; JAHNKE et al., 1990). The comparison and modelling of O2 uptake from different regions is further complicated by the fact that the particle flux and 02 uptake of deep sea sediments exhibit significant seasonal (SMITHand BALDWIN,1984; NAIR et al., 1989) and interannual (DEUSER,1986) variations. However, other data also confirm that eastern upwelling regions have substantially higher 02 uptake

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rates than central or western non-upwelling regions of the oceans (JAHNKEand JACKSON, 1987; JAHNKEet al., 1989). Differences between data obtained in situ and in the laboratory

The data presented in this paper consistently show that 02 profiles measured in sediment cores recovered from water depths of more than 1.0 km had changed significantly compared to profiles measured in situ. The 02 penetration depths were shallower, and the 02 concentration gradients in the DBL and in the upper part of the sediment were steeper, when profiles were measured in the laboratory. The difference increased when the water depth increased. It has been reported previously that O2 uptake rates measured in the laboratory were higher than those measured in situ (SMITHand HIN~A, 1983; SMITHet al., 1983; REIMERSet al., 1986; JAHNKEet al., 1989). Several possible mechanisms explaining the differences have been suggested: disturbance of the sediment surface during sampling; compression of the sediment matrix during coring; decompression effects on pore water chemistry; pore water expansion due to decompression; decompression effects on microbial activity; destruction of organisms by decompression, thereby increasing the availability of labile organic material; or temperature changes during recovery. Micro pH-profiles measured in recovered sediment cores showed a distinct minimum at a depth corresponding to the 02 penetration depth measured in situ (DAHMKE et al., unpublished manuscript). A pH minimum at the oxic-anoxic interface is to be expected, and the fact that the conservative pH profile matches the in situ 02 penetration depth argues against the interpretation that a compression of the whole sediment during coring can explain the altered 02 profiles. Water is compressed by the hydrostatic pressure; e.g. at 4.0 km depth by about 2% (KELL, 1975). During recovery of the sediment core, the pore water expansion will result either in an expulsion of pore water or an expansion of the entire core. If the entire core length expanded, the 02 penetration depth would be expected to increase, and the concentration gradient in the DBL would decrease. We observed the opposite effect. However, expelling of pore water due to release of the hydrostatic pressure would have the observed effect on the 02 profiles, and the effect would increase with increasing water depth. Calculations showed, however, that an expulsion of pore water could only account for 5-25% of the observed change in 02 penetration depth. The change in the 02 profiles could also have been caused by a transient heating of the sediment cores during recovery and handling on deck. Such an increase in temperature would stimulate the respiration processes and thereby increase the 02 uptake and decrease the O2 penetration depth. A combined effect of decompression and increased temperature can inactivate and even be lethal to some psycrophilic and barophilic bacteria and meiofauna (YAYANOSand DIETA, 1982; SMITHand HINGA, 1983; TURLEYet al., 1988). An increase in microbial activity after decompression due to increased availability of organic compounds as a result of lysis of baro- and temperature-sensitive bacteria and meiofauna could further enhance the 02 uptake. After placement of the cores at in situ conditions in the incubation tank, diffusion would gradually reestablish the original pore water profile. With an 02 penetration of several cm it would, however, take days before steady state reoccurred, and we preincubated only for 3 h. The appropriate preincubation time is thus a balance between allowing the sediment cores to recover from transient disturbances and avoiding changes in bacterial populations


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a n d o t h e r f a c t o r s d u e to p r o l o n g e d s t o r a g e . I n c o n c l u s i o n , w e a s c r i b e t h e d i f f e r e n c e b e t w e e n 0 2 profiles o b t a i n e d in situ a n d in t h e l a b o r a t o r y to a c o m b i n a t i o n o f e x p u l s i o n o f p o r e w a t e r a n d d e c o m p r e s s i o n a n d t e m p e r a t u r e effects on m i c r o b i a l m e t a b o l i s m . A t t h e s t a t i o n s with a s p a r s e f a u n a , t h e t o t a l 0 2 u p t a k e m e a s u r e d in t h e l a b o r a t o r y was h i g h e r t h a n t h a t m e a s u r e d in situ, as was t h e case with t h e diffusive 0 2 u p t a k e ( T a b l e s 2 a n d 3). H o w e v e r , at t h e s h a l l o w , f a u n a - r i c h s t a t i o n s , t h e t o t a l 0 2 u p t a k e m e a s u r e d in t h e l a b o r a t o r y was l o w e r t h a n t h a t m e a s u r e d in situ. This is p r o b a b l y d u e to t h e fact t h a t t h e f a u n a d e n s i t y in s e d i m e n t c o r e s was l o w e r t h a n in t h e c h a m b e r o f E L I N O R ( T a b l e 3). It is difficult to i n c l u d e fully t h e effect o f m a c r o f a u n a o n t h e e x c h a n g e r a t e s in small s e d i m e n t c o r e s , since l a r g e r s p e c i e s will o f t e n n o t b e p r e s e n t in successfully r e c o v e r e d , visibly u n d i s t u r b e d s e d i m e n t c o r e s , a n d , if t h e y a r e p r e s e n t , t h e a n i m a l s o r t h e i r b u r r o w s t r u c t u r e s a r e o f t e n d i s t u r b e d o r d e s t r o y e d . F u r t h e r , s m a l l e r s e d i m e n t c o r e s will b e m o r e a f f e c t e d b y e d g e effects, a n d local h e t e r o g e n e i t y will to less e x t e n t b e l e v e l l e d o u t t h a n in l a r g e r cores. T h e c h a m b e r o f E L I N O R h a r b o u r s a m o r e intact a n d u n d i s t u r b e d f a u n a b e c a u s e o f its l a r g e r s a m p l i n g a r e a , a n d t h e f a u n a is n o t d e c o m p r e s s e d b e f o r e i n c u b a t i o n . M e a s u r e m e n t s in c o a s t a l , f a u n a - r i c h s e d i m e n t s h a v e also s h o w n t h a t l a b o r a t o r y incub a t i o n s u n d e r e s t i m a t e t o t a l in situ 0 2 u p t a k e (GUNDERSEN et al., u n p u b l i s h e d m a n u script). In c o n c l u s i o n , t h e t w o o p p o s i n g effects on O2 u p t a k e m e a s u r e m e n t s d e m o n s t r a t e t h a t in situ m e a s u r e m e n t s a r e n e c e s s a r y to u n d e r s t a n d c o r r e c t l y t h e e a r l y d i a g e n e s i s a n d O2 d y n a m i c s o f t h e d e e p - s e a floor. Acknowledgements--We thank A. Dahmke, U. Werner, J. Sagemann and K. Dehning for their great help during the cruise and the captain and crew of the R.V. Meteor for their assistance. In addition we thank A. Glud and L. B. Pedersen for construction of microelectrodes. Unpublished data on organic carbon concentrations were kindly supplied by P. Miiller. This research was supported by the Danish Environmental Protection Agency (Marine Research Program 90) and the "Deutsche Forschungsgemenschaft" (Special project of the German Science Foundation "The South Atlantic in the late quaternary: Reconstruction of material budget and current system"; publication no. 63).

REFERENCES ALLERR. C. (1978) Experimental studies of changes produced by deposit feeders on porewater, sediment and overlying water chemistry. American Journal of Science, 278, 1185-1234. ALLERR. C. and J. Y. YINGST(1985) Effects of marine deposit-feeders Heteromastusfiliformis (Polychaeta), Macoma baltica (Bivalvia), and Tellina texana (Bivalvia) on averaged sedimentary solute transport, reaction rates, and microbial distribution. Journal of Marine Research, 43, 615-645. ARCHERD. and A. DEVOL(1992) Benthic oxygen fluxes on the Washington shelf and slope: a comparison of in situ microelectrode and chamber flux measurements. Limnology and Oceanography, 37,614-629. ARCHERD., S. EMERSOMand C. E. REIMERS(1989) Dissolution of calcite in deep-sea sediments: pH and 02 microelectrode results. Geochimica et Cosmochimica Acta, 53, 2831-2845. ARCHERD., S. EMERSONand C. R. Surrn (1989) Direct measurement of the diffusive sublayer at the deep sea floor using oxygen microelectrodes. Nature, 340, 623--626. BARNETTP. R. O., J. WATSONand D. CONNELLY(1984) A multiple corer for taking virtually undisturbed samples from shelf, bathyal and abyssal sediments. Oceanologica Acta, 7, 399-408. BERGERW. H., K. FISCHER,C. LAI and G. Wu (1987) Ocean productivity and organic carbon flux. Part I. Overview and maps of primary production and export production. SIO Reference Series, 87-30, 67 pp. BROECKERW. S. and T. H. PENG(1974) Gas exchange rates between air and sea. Tellus, 26, 21-35. CANFIELD D. E. (1992) Organic matter oxidation in marine sediments. In: Interactions of C,N,P and S biochemical cycles, R. WOLLAST,L. CHOUand F. MACKENZIE,editors, Nato-ARW. Springer Verlag, pp. 333-363. CARPENTERW. B. (1869) On the rhizopodalfauna of the deep sea. The Royal Society, London, England, 18, 60.

1786

R . N . GLUD et al.

CRAMER A. (1989) A c o m m o n artefact in estimates of benthic community respiration caused by the use of stainless steel. Netherlands Journal of Sea Research, 23, 1~6. CRANK J. (1983) The mathematics of diffusion. Clarendon Press, Oxford, 372 pp. DEMASXER D. J. and J. K. COCHRAN(1982) Particle mixing rates in deep-sea sediments determined from excess 21°Pb and 32Si profiles. Earth and Planetary Science Letters, 61,257-271. DEUSER W. G. (1986) Seasonal and interannual variations in deep-water particle fluxes in the Sargasso Sea and their relation to surface hydrography. Deep-Sea Research, 33,225-246. GRAF G., W. BENGTSSON, U. DIESNER, R. SCHULZ and H. THEEDE (1982) Benthic response to sedimentation of a spring phytoplankton bloom: process and budget. Marine Biology, 67,201-208. GLUD N. R., J. K. GUNDERSEN, B. B. JORGENSEN and N. P. REVSBECH(1994) Effects on the benthic diffusive boundary layer imposed by microelectrodes. Limnology and Oceanography 39,462-467. GLUD N. R., J. K. GUNDERSEN, N. P. REVSBECHand B. B. JORGENSEN (in press) In situ measurements of total and diffusive oxygen uptake of sediments. Proceedings of the 6th International Symposium on Microbial Ecology', Barcelona, 1992. GRUNDMAN1S V. and J. W. MURRAY (1977) Nitrification and denitrification in marine sediments from Puget Sound. Limnology and Oceanography, 22,804-813. GUINASSO JR N. L. and D. R. SCHINK (1975) Quantitative estimates of biological mixing rates in abyssal sediments. Journal of Geophysical Research, 80, 3032-3043. GUNDERSEN J. K. and B. B. JORGENSEN(1990) Microstructure of diffusive boundary layers and the oxygen uptake of the sea floor. Nature, 345,604-607. GUNDERSEN J. K. and B. B, JORGENSEN (1991) Fine-scale in situ measurements of oxygen distribution in marine sediments. Kieler Meeresforschung, 8, 376-380. HALl, P. O. J., L. G. ANDERSON, M. M. RUTGERSVAN DER LOEFF, B. SUNI)BY and S. F. G. WES'IERLUND (1989) Oxygen uptake kinetics in the benthic boundary layer. Limnology and Oceanography, 34,734-746. HESSLER R. R. and P. A. JUMARS(1974) Abyssal community analysis from replicate box cores in the central North Pacific. Deep-Sea Research, 21, 185-209. HOTrEt, M. and G. G u s t (1992) Solute release mechanisms from conlined sediment cores in stirred benthic chambers and flume flows. Marine Ecology Progress Series, 82, 187-197. JAHNKE R. A. and M. B. CHRISTIANSEN(1989) A free-vehicle benthic chamber instrument for sea floor studies. Deep-Sea Research, 3 6 , 6 2 5 ~ 3 7 . JAHNKE R. A., S. R. EMERSON, J. K. COCHRANand D. J. HIRSCHBERG(1986) Fine scale distribution of porosity -"~ -910ph and particu ate exccs~ ,L,, org"anlc " carbon and C a C O 3 in surface sediments of the deep equatorial Pacific. Earth and Planetary Science Letwrs, 77, 5 9 ~ 9 . JAHNKE R. A., S. R. EMERSON, C. E. REIMERS, J. SCHUFFER1. K. RU3q'ENI~ERGand I). ARCHER (1989) Benthic recycling of biogenic debris in the eastern Atlantic Ocean. Geochimica et Cosmochimica Acta, 53, 29472960. JAHNKE R. A., D. HEGGm, S. EMERSON and V. GRUNDMANIS(1982) Porc waters oi' the central Pacific Ocean: Nutrient results. Earth and Planetary Science Letters, 61,233-256. JAHNKE R. A. and G. A. JACKSON (1987) Role of sea floor organisms in oxygen consumption in the deep North Pacific Ocean. Nature, 329, 621-623. JAHNKE R. A., C. L. REIMERS and D. B. CRAVEN (1990) Intensification of recycling of organic matter at the sea floor near ocean margins. Nature. 348, 50-54. JANNASCHH. W. and C. D. TAYLOR(1984) Deep sea microbiology. Annual Review of Microbiology, 38,487-514. JORGENSEN B. B. and D. MARAIS(1990) The diffusive boundary layer of sediments: oxygen microgradients over a microbial mat. Limnology and Oceanography, 35, 1343-1355. JORGENSEN B. B. and N. P. REVSBECH (1985) Diffusive boundary layers and oxygen uptake of sediments and detritus. Limnology and Oceanography, 30, 111-122. KANNEWORF E. and H. CHRmTENSEN (1986) Benthic community respiration in relation to sedimentation of phytoplankton in the Oresund. Ophelia, 26, 269-284. KELL G. S. (1975) Density, thermal expansivity, and compressibility of liquid water from 0 ° to 150°C: correlations and tables for atmospheric pressure and saturation reviewed and expressed on 1968 temperature scale. Journal of Chemical and Engineering data, 20, 97-105. KRISTENSEN E. (1985) Oxygen and inorganic nitrogen exchange in a Nereis virens (Polychaeta) bioturbated sediment-water system. Journal of Coastal Research, 1,109-116. LI Y. H. and S. GREGORY(1974) Diffusion of ions in deep-sea sediments. Geochimica et ('~smochirnica Acta, 38, 703-714.


1787

NAIR R. R., V. ITrEKKOT,S. J. MANGANINI,V. RAMASWAMY,B. HAAKE,E. T. DEGENS,B. N. DESAIand S. HONJO (1989) Increased particle flux to the deep ocean related to monsoons. Nature, 338, 749-751. NIELSEN L. P., P. B. CHRISTENSEN, N. P. REVSBECH and J. SORENSEN (1990) Denitrification and oxygen respiration in biofilms studied with a microsensor for nitrous oxide and oxygen. Microbial Ecology, 19, 6372. NOSHKINV. E. and V. T. BOWEN(1973) Concentrations and distributions of long-lived fallout radionuclides in open ocean sediments. In: Radioactive Contamination of the Marine Environment, pp. 671-686, International Atomic Energy Agency, Vienna. PAMATMAT M. M. (1971) Oxygen consumption by the seabed IV. shipboard and laboratory experiments. Limnology and Oceanography, 16,536-550. PATCHINGJ. W., R. C. T. RAINE, P. R. O. BARNETtand J. WATSON(1986) Abyssal benthic oxygen consumption in the Northeast Atlantic: measurements using the suspended core technique. Oceanologica Acta, 9, 1-7. RASMUSSEN H. and B. B. JORGENSEN (1992) Microelectrode studies of seasonal oxygen uptake in a coastal sediment: role of molecular diffusion. Marine Ecology Progress Series, 81,289-303. REIMERS C. E. (1987) An in situ microprofiling instrument for measuring interfacial pore water gradients: methods and oxygen profiles from the North Pacific Ocean. Deep-Sea Research, 34, 2019-2035. REIMERSC. E. and K. L. SMITH(1986) Reconciling measured and predicted fluxes of oxygen across the deep sea sediment-water interface. Limnology and Oceanography, 31,305-318. REIMERS C. E., K. M. FISCHER, R. MEREWETHER,K. L. SMITHand R. A. JAHNKE(1986) Oxygen microprofiles measured in situ in deep ocean sediments. Nature, 320, 741-744. REVSBECHN. P. (1989a) An oxygen microelectrode with a guard cathode. Limnology and Oceanography, 34, 474-478. REVSBECH N. P. (1989b) Diffusion characteristics of microbial communities determined by use of oxygen microsensors. Journal of Microbial Methods, 9, 111-122. REVSBECHN. P. and B. B. JORGENSEN(1986) Microelectrodes and their use in microbial ecology. In: Advances in microbial ecology, 9, K. C. MARSHALL,editor, Plenum, New York, pp. 293-352. SCHINK D. R. and N. L. GUINASSOJR (1976) Effects of bioturbation on sediment-seawater interaction. Marine Geology, 23,133-154. SCHULZ H. D. et al. (1992) Berichte und erste Ergebnisse iiber die Meteor-Fahrt M20/2 Abidjan-Dakar, 21, 12, 1991-3, 2, 1992 Berichte, Fachbereich Geowissenschaften, 25, 48. SMITHJR K. L. (1978) Benthic community respiration in the N.W. Atlantic Ocean in situ measurements from 40 to 5200 m. Marine Biology, 47,337-347. SMITH JR K. L. (1987) Food energy supply and demand: a discrepancy between particulate organic carbon flux and sediment community oxygen consumption in the deep ocean. Limnology and Oceanography, 32,201220. SMITH JR K. L. and R. J. BALDWIN (1984) Seasonal fluctuations in deep-sea sediment community oxygen consumption: central and eastern North Pacific. Nature, 307, 624-625. SMITHJR K. L. and K. R. HINGA(1983) Sediment community respiration in the deep sea. In: The sea, Vol. 8, G. T. RowE, editor, pp. 331-370. Wiley, New York. SMITHJR K. L., M. B. LAVERand N. O. BROWN(1983) Sediment community oxygen consumption and nutrient exchange in the central and eastern North Pacific. Limnology and Oceanography, 28, 882-898. SMITHK. L., G. A. WHITEand M. B. LAVER(1979) Oxygen uptake and nutrient exchange of sediments measured in situ using a free vehicle grab respirometer. Deep-Sea Research, 26,337-346. STRICKLANDJ. D. and T. R. PARSON(1972) A practical handbook of seawater analysis, 2nd edn, Bulletin of the Fish Research Board of Canada, 167, 310 pp. SWEERTSJ. P. R. A., V. ST LOUIS and T. E. CAPPENBERG(1989) Oxygen concentration profiles and exchange in sediment cores with circulated overlying water. FreshwaterBiology, 21,552-556. THORPE S. A. and M. WHIT (1988) A deep intermediate nepheloid layer. Deep-Sea Research, 35, 1665-1671. TURLEYC. M., K. LOCHTEand D. J. PATrERSON(1988) A barophilic flagellate isolated from 4500 m in the midNorth Atlantic. Deep-Sea Research, 35, 1079-1092. ULLMAN W. J. and R. C. ALLER (1982) Diffusion coefficients in nearshore marine sediments. Limnology and Oceanography, 27, 552-556. VOGEL S, (1981) Life in moving fluids. Princeton, New Jersey. WEAVERP. P. E. and P. J. SCHULTHEISS(1983) Vertical open burrows in deep-sea sediments 2 m in length. Nature, 301,329-331.

1788

R.N. GLUD et al.

WILSON T. R. S., J. THOMSON, S. COLLEY,D. J. HYDESand N. C. HIGGS (1985) Early organic diagenesis: the significance of progressive subsurface fronts in pelagic sediments. Geochimica et Cosmochimica Acta, 49, 811-822. YAYANOSA. A. and A. S. DIETZ (1982) Thermal inactivation of a deep-sea barophilic bacterium, isolate CNPT-3. Applied and Environmental Biology, 43, 1481-1489.