Publication 2680 Netherlands Institute of EcologyCentre for Estuarine and Coastal Ecology, Yerseke,The Netherlands

Vol. 215: 13-22.2001 Published May 31MARINE ECOLOGY PROGRESS SERIES

Mar Ecol Prog Ser

Effect of oxygen on the degradability of organicmatter in subtidal and intertidal sediments of

the North Sea area

Birgit Dauwe*, Jack J. Middelburg**, Peter M. J. Herman

Netherlands Institute of Ecology. Korringaweg 7. 440I NT Yerseke, The Netherlands

ABSTRACT: The effect of oxygen on the degradation of sedimentary organic matter has been deter-mined for 6 sub tidal stations and 3 intertidal stations in the North Sea area. The stations wereselected to cover a range of organic matter lability and sediment texture (and hence concentrationsof organic matter). Slurry incubations revealed that at low mineralisation rates, aerobic mineralisa-tion is significantly faster than anaerobic mineralisation, irrespective of the degree of lability oforganic matter. A complementary incubation experiment with sediment rich in organic carbon mixedwith varying proportions of organically poor sediments confirmed the enhanced aerobic mineralisa_tion at low mineralisation levels. It is proposed that oxygen-enhanced degradation occurs at low min-eralisation levels at which bacterial biomass production becomes limiting.

KEYWORDS: Organic matter. Degradation. Oxygen. Sediments . North Sea. Intertidal

Resale or republication not permitted without written consent of the publisher

INTRODUCTION

In most coastal sediments. aerobic decomposition islimited to the upper few millimetres and to the wallsof ventilated animal burrows (Aller 1982), whereasanaerobic decomposition is the major mineralisationprocess in the deeper layers of the sediment column(J0rgensen 1983). The influence of sedimentary redoxconditions on mineralisation rates is still a matter of

debate. Knowledge of the effect of oxygen on thedegradability of organic matter is required to betterdefine the factors governing' the preservation oforganic matter in marine sediments (Canfield 1994.Hartnett et al. 1998. Hulthe et al. 1998). Decompositionof organic matter is usually modelled as having a first-order or higher-order (Westrich & Berner 1984. Mid-delburg 1989) dependence on organic matter content.independent of oxidant availability and bacterial bio-

*Present address: RIKZ. Postbus 8039.4330 EA Middelburg.The Netherlands

**Corresponding author.E-mail: middelburg@cemo.nioo.knaw.nl

@ Inter-Research 2001

- - - --

mass (Boudreau 1999). If oxygen affects the degrad-ability of organic matter.. this will require revision ofdiagenetic models. Moreover, benthic animals mayrapidly displace organic material from the oxic to theanoxic layers of sediments and vice versa (Aller 1994).Hence, these organisms could thus affect the degrad-ability of organic matter (AlIer & Aller 1998).

Much effort has consequently been devoted to deter-mining whether aerobic mineralisation is faster thananaerobic mineralisation. Even though there is experi-mental evidence that mineralisation rates oflabile sed-

imentary organic matter are not significantly differentunder oxic and anoxic conditions (e.g. Westrich &Berner 1984. Canfield 1989, Lee 1992, Andersen 1996),other studies have shown that some (refractory) com-pounds of the organic matter degrade more slowlyunder anoxic than under oxic conditions (Hansen &Blackburn 1991. Sun et al. 1993a.b. Cowie et al. 1995.Harvey et al. 1995. Hulthe et al. 1998). Other experi-mental studies have come to the conclusion that anaer-

obic processes may even be faster than aerobic pro-cesses (e.g. Kristensen & Blackburn 1987. Hulthe et al.1998). It has been suggested that the lability of organic

14 Mar Ecol Prog Ser 215: 13-22, 2001

matter determines its relative susceptibility to aerobicversus anaerobic decay (Hulthe et al. 1998). but alsosource differences (even though they may be co-related to quality) probably play a role (Benner et al.1984. Kristensen et al. 1995),

Geoscientists have reported field evidence of aneffect of oxygen on organic matter degradation on longtime scales, Wilson et al. (1985) observed that organicmatter in a relict deep-sea turbidite from the Madeiraabyssal plain exhibited little degradation over a140000 yr period when exposed to sulphate. but that80% of the carbon was respired within 10000 yr in thepresence of oxygen, Canfield (1994) presented evi-dence that preservation of organic matter was depend-ing on bottom-water oxygen concentrations at low.but not at high. sediment accumulation rates. Morerecently. Hartnett et al. (1998) gave correlative evi-dence that the period of time that organic matteris exposed to oxygen determines the efficiency ofthe mineralisation processes. Sediment accumulationrates and oxygen exposure times comprise manyfactors known to affect mineralisation on decadal andmillennial time scales.

Most experimental results and field studies supportthe hypothesis that the quality of the organic mattercontrols whether oxygen affects the mineralisationprocess. However. sedimentS with more refractoryorganic matter showing an oxygen-dependent degrad-ability usually also have low organic matter concentra-tions. with the result that mineralisation rates are alsolow, We hypothesise that there is a critical level of min-eralisation of organic matter below which aerobicdegradation is faster than anaerobic degradation. Inmarine sediments. the concentration and lability oforganic matter often co-vary because they both de-crease upon degradation. To uncouple the effect of

organic matter lability and mineralisation level fromthe oxygen dependence of mineralisation. we havemade a cross-system study in coastal sediments of theNorth Sea area. Six subtidal stations and 3 intertidal

stations were selected to cover a range of organic mat-ter of various lability and sediment texture (and henceconcentrations of organic matter) (Dauwe & Middel-burg 1998. Dauwe et al. 1999). Moreover. sedimentthat was rich in organic matter from 1 intertidal sitewas mixed with sediment of low organic matter con-tent to lower the mineralisation level while maintain-

ing the quality of the organic matter constant.

MATERIALSAND METHODS

Sampling. Sediment samples were taken from 6 sub-tidal stations in the North Sea in November 1995

.<Fig. 1. Table 1: Stns Skagerrak (SK]. German Bight(GB]. Friesian Front (FF]. Broad Fourteens (BF)) and inMay 1996 (Brouwershavensche-gat (Stns BG-A. BG-B)). Three intertidal stations were sampled in June1996. 2 located on a tidal flat in the Westerschelde(Molenplaat: (Stns Mol-2 and Mol-3)) and 1 on a mus-selbank in the Oosterschelde {Stn Zandkreek (ZK))(Fig. 1. Table 1). At the North Sea stations. most freshorganic matter originates from the deposition of phy-toplankton blooms. The sedimentary organic matterreflects a broad sequence of different organic matterdegradation states. probably due to ageing during lat-eral bed-load transport with residual currents and dif-ferences in water depth (Dauwe & Middelburg 1998).In the intertidal areas. fresh organic matter input isdominated by primary production of benthic micro-algae at Stns Mol-2 and Mol-3 (Barranguet et al. 1997)and strong biodeposition of organic matter as faeces on

Table 1. Characteristics of sampling stations (labelled as in Fig. 1) and conditions of the incubation experiments, Values in paren-theses are for surface 0 to 1 cm layer of sediment

-- - -- - - - - ---- ---

Stn Latitude Longitude Depth Sediment Incubation(m) Median TOe Sampling Incubation r Gas pH

grain size (wt%) period period (d) ("C)(pm) Oxic Anoxic Oxic Anoxic Oxic Anoxic

SubtidalGB 8" 09' E 54" OS' N 20 (l6) 31 1.12 Noy 95 21 22 16 NiOz Nz 6.9:1:0,3 7.1:1:0.1SK 10" IS' E 58" 12' N 270 (13) 12 2.47 Noy 95 19 20 16 Nz/Oz Nz 6.6:1:0,3 7.3 :I:0.1FF 4° 30' E 53° 42' N 39 (40) 83 0.51 Noy 95 20 21 16 NiOz Nz .7.1 :I:0.05 7,2:1:0.07BF 3° 52' E 53° 00' N 28 (266) 248 0.05 Noy 95 22 22 16 Nz/Oz Nz 7.0:1:0,15 7.1 :I:0.04BG-A 3° 48' E 51°45' N 5 (162) 185 0.16 May 96 27 27 16 Nz/Oz Nz 6.9 :1:0.1 7.3:1:0.24BG-B 3" 46' E 51°46'N 3 (305) 354 0.02 May 96 27 27 16 Nz/Oz Nz 7.0:1:0.07 7.3:1:0.13

IntertidalMol-2 3"57'2' E 51"26'3' N - (70) 120 0.52 lun 96 22 22 16 Nz/Oz Nz 6.9:1:0.15 7.4 :I:0,16Mol-3 3" 56' 9' E 51° 26' 25' N - (160) 180 0.18 lun 96 22 22 16 NiOz Nz 7.0:1:0.23 7.3 :1:0.15ZK 3" 5 4' E 51" 33' N - (238) 190 0.25 lun 96 29 29 16 Nz/Oz Nz 7.3:1:0.08 6.9 :1:0.1

Dauwe et a!.: Effect of oxygen on degradation of organic matter 15

4° 0° 4' 8° 12°

58'

North Sea56'

54° FFo

52'

50'

screw caps provided with rubber septa.This resulted in a slurry:headspace ratioof 30:40 ml. Headspaces were purged 3times for 10 min with Nz for the anoxicincubations and with Nz:Oz (80:20) for

the oxic incubations. Between flushings.the slurries were shaken and allowed to

equilibrate for 10 min. Bottles containingonly gas and bottles containing gas andfiltered seawater were used as controls.

Final changes in control flasks withoutsediment were always < 3 % of initialconcentrations. Other controls contain-

ing sediment and water were poisonedby adding 1 ml of 1% HgCI. There was

. no significant COz release from poisonedsediments. CH4 release in the anoxic in-cubations was maximally 2 % of COz re-lease. and was therefore ignored. Duringthe whole incubation period. the flaskswere continuously rotated. allowing anoptimal exchange between the slurryand the headspace gas (van der Nat etal. 1997). All slurries and controls wereincubated in the dark at 16°C for about

20 to 30 d (fable 1). This length of incu-bation was necessary to ensure sufficientaccuracy for low-activity samples. A se-lection of samples covering the entire ac-tivity range was incubated lO-fold underoxic and anoxic conditions to study thekinetics of degradation. COz productionrates were linear for >40 d (Fig. 2). con-sistent with observations by Hulthe et al.(1998).

Headspace concentrations of COz. Oz and CH4 weredetermined using a Carlo Erba high-resolution MEGA5340 gas chromatograph. equipped with a flame ioni-

Fig. 1. Locations of sampling stations. (A) North Sea stations: SK =Skagerrak:GB =German Bight; FF =Friesian Front; BF = Broad Fourteens; BG =Brou-wershavensche gat A and B. (B) Intertidal stations: Mol = Molenplaat 2 and 3:

ZK = Zandkreek

the sediments by mussels at Stn ZK (Herman et al.1999). Samples of the subtidal sediments were ob-tained with a cylindrical Reineck-type box corer (31 cmi.d. (inner diameter». and subsampled using acrylictubes (60 cm length. 3.3 cm i.d.). The intertidal StnsMol-2. Mol-3 and ZK were sampled by direct coringwith acrylic tubes. At each station. 4 subcores weresliced and then pooled per depth stratum and thenmixed. All macrofauna and shell fragments wereremoved prior to incubation. At Stns Mol-2 and Mol-3.replicate sediment oxygen-consumption rates weremeasured using a shipboard core-incubation tech-nique (Moodley et al. 1998).

Degradability of organic matter. Degradability of or-ganic matter was assessed by measuring the productionof COz and CH4. the end products of carbon mineralisa-tion. in the headspace above sediment-water slurries. Avolume of -20 ml sediment was transferred into 70 ml

glass incubation bottles (Chrompack). and diluted with10 ml filtered seawater; the bottles were sealed with

a. Oxic: R2 = 0.87Anoxic: R2 = 0.78

.[J..'

a ....... ..

10 20 30

Time (d)

40 50

Fig. 2. Example of the evolution of C02 produced during anoxic and an anoxic incubation. Regression lines and coeffi-

cients of determination are shown

12

10

8Cl

15E 6.:...0 4U

2

00

sation detector. a hot wire detector. a methaniser and a

3 m Haysep-Q and 2 m molsieve column. At the end ofthe incubations. the vials were opened and the pH wasmeasured. The samples were weighed. freeze-dried.and weighed again in order to determine the dryweight and exact volume of the incubated sediment.

The total amount of gas produced or remaining inthe incubation bottles was calculated as the sum of the

headspace and dissolved concentrations. Equilibrium

-----

concentrations of the gases in the sediment-water slur-ries are based on measured headspace concentrationsand temperature- and salinity-dependent solubilitycoefficients. For C02. the pH-dependent speciationwas also taken into account (Stumm & Morgan 1996).All mineralisation rates were expressed as J.1molC02(g dry sediment)-I d-I, abbreviated as J.1molC g-I d-I.Analytical reproducibility of total C02 measurementsis about 5%. taking into account inherent uncertainties

-- -

Dauwe et a!.: Effect of oxygen on degradation of organic matter 17

in COz gas measurements in the head space and inslurry pH measurements.

COz production generally resulted in some acidifi-cation at the end of the experiment during aerobicmineralisation compared to the anoxic incubations(Table I), probably due to the buffering capacity ofmany of the anaerobic reaction products (e.g., HC03-,HzSand NH4+) and sulphide oxidation in the oxic incu-bations. The oxygen concentration in the oxic slurrieswas 234 JImoll-1 at the beginning of the incubation and15 to 80 JImoll-1 after 3 wk at the stations with highmineralisation rates (Stns SK and GB); this is wellabove the 3 JImoll-1 which comprises the half-satura-tion constant for Oz limitation in aerobic mineralisation(Gaillard & Rabouille 1992).

Preparation of sediment mixture. Surface sediment(0 to 1 cm) was collected at the intertidal Stn Mol-2 onNovember 23, 1998. The sediment was freeze-driedand diluted to 25, 6.25, 1.56 and 0.39% by adding anorganically poor sediment mixture (0.03 wt%) of extrapure sand (Merck) and freeze-dded North Atlanticdeep-sea sediment (3:1). The sand:silt ratio of theadded mixture was similar to that of the intertidalsediment. These sediment mixtures were incubated

as in the preceding subsection. Two replicates wereincubated for each of the 3 incubation periods (20, 23,31 d).

Sediment parameters. Sediment parameters weredetermined for a subsample of the initial sample.Median grain sizes were determined for freeze-driedsamples with a Malvern Particle Sizer 3600 EC. Poros-ity was calculated from water content (weight loss ondrying at 100°C) assuming a dry density of 2.5 kg dm-3for sediment. After iD situ acidification with 25% HCI

in precleaned silver cups to remove inorganic carbon(Nieuwenhuize et al. 1994), organic carbon concentra-tions were determined as total carbon.

RESULTS

At most stations, carbon dioxide productiondecreased strongly with increasing depth, except atStn BF (Fig. 3). Very steep profiles were found at theintertidal Stns Mol-2, Mol-3 and ZK (>90% decreasewith respect to surface mineralisation), whereas therates at Stns SK, FF, BG-A and BG-B decreased more

gradually (60 to 75% of original surface concentrationat 5 cm depth). At Stn GB, degradable carbon initiallyincreased with increasing depth and then decreased(Fig. 3B). Depth-integrated (0 to 15 cm) carbon dioxideproduction. based on the average of oxic and anoxicincubation, varied from 12 to 140 mmol m-2 d-I

(Fig. 4A); the sequence was: Mol-2 > ZK = GB = Mol-3> BG-A > SK = FF > BG-B = BF.

Vertical profiles measured under oxic and anoxicconditions had similar shapes at most stations (Fig. 3).except at Stn BF where the aerobic profile showed anextended subsurface peak, whereas the anaerobic pro-file remained constant with depth. The consistent dif-ferences between carbon dioxide production underoxic and anoxic conditions over the entire sediment

depth (Fig. 3) were reflected by the ratio of aerobicversus anaerobic mineralisation rates based on depth-integrated COz production (Fig. 4B). The aerobic min-eralisation rate was significantly higher than theanaerobic rate at the coarse-grained Stn FF (n = 13, P <0.001), BF (n = 13, P < 0.001), and BG-B (n = 11, P <0.001) sediments, with ratios of aerobic rate versusanaerobic rate of between 1.7 and 2.7. At the other sta-tions, aerobic and anaerobic mineralisation rates weresimilar (Stns GB, BG-A, Mol-2, Mol-3) or anaerobicrates were even slightly higher (Stn SK, n = 12, P =0.03; Stn ZK, n = 12, P = 0.003).

A log-log plot of aerobic versus anaerobic minerali-sation rate is given for all sediments that had an oxy-gen concentration of more than 80 JImol O2 I-I at theend of the oxic incubations (Fig. 5A). The slope of thegeometric mean regression line (1.41 j: 0.074) is signif-icantly different from 1 (Student's I-test, n = 57, P <:0.001), indicating that mineralisation rates ofsedimen-tary organic matter are different under anoxic com-pared to oxic conditions. Although the differences atintermediate to high mineralisation rates were mar-

(B) subtidal intertidal(.) 3:0e~ 2c:as.2,.co"-IDas 0

GB SK FF BF BG-A BG-8 MOI.2 MoI.3 ZK

Fig. 4. (A) Depth-integrated (0 to 15 cm) carbon dioxide pro-duction (X :I: SD aerobic and anaerobic mineralisation):(B) ratio of depth-integrated aerobic versus anaerobic miner-alisation. Sampling stations (abscissas) labelled as in Fig. I

--

'0 (A) subtidal intertidal

150E'0 125E

100.sCD 75"'x 500'6c 250

0III0 GB SI< FF BF BG-A 00-8 MoI-2 MoI-3 ZJ(

18 Mar Ecol Prog Ser 215: 13-'22, 2001

'-..-b..-'0)o(3E::1.

--- 0.1(J:ceQ)COc:« 0.01

. 100%° 25%. 6.25%o 1.56%.. 0.39%

- - geometric OMan-':11ne

./

/

.. //. oJlo °.t:0/

//

/(B)

0.01 0.1

- 1:1line(E=A=1)- - A= 0.03;E = 1

... A =0.01; E= 1-.. - A = 0.03; E = 0.5

(C)

0.01 0.1

Aerobic (~ol C 9-1 d-1)

Fig. 5. Log-log plots of aerobic versus anaerobic mineralisa-tion rates. (A) Sedimentary organic matter from Stns SK, FF,BF and BG-B. at all depth intervals (SK*: data from Hulthe etal. [1998]: see 'Discussion'), showing 1:1 and geometric meanregression lines; (B) dilution experiment with percentage oforiginal sediment. showing 1:1 and geometric mean regres-sion lines; (C) model results for A =0.03. E = 1;A = 0.01, E = 1;

and A = 0.03. E = 0.5 (A = constant; E = efficiency factor)

ginal. at low mineralisation rates «0.1 ~mol C g-I d-I),typical for the sandy Stns BF and BG-B (Fig. SA). aero-bic mineralisation was up to 50% higher than ratesmeasured under anoxic conditions.

Fig. 6. Ratio between measured aerobie and anaerobic miner-alisation rates as a function of the labilityof organic carbon(defined as the mineralisation rate divided by the organic car~bon content of the sedimentary organic matter). TOC: total

organic carbon

To investigate whether the observed differences be-tween aerobic and anaerobic mineralisation rates cor-

related with the lability of the organic matter, the ratio ofaerobic versus anaerobic rate was plotted against the

la~ility of the organic matter expressed as the amount ofcarbon mineralised per gram total organic carbon (TOe)per day (Fig. 6). There was no clear trend in the ratio overthe large range of lability measured for sedimentaryorganic matter (-10 to >600 J.1molC g-I TOC d-I).

During incubation of the sediment dilution series,dissolved oxygen concentrations were always above140 ~M. Fig. 5B shows the log-log plot of aerobic ver-sus anaerobic degradation. Again, the slope of the geo-metric lJlean regression (1.77 % 0.19) is significantlydifferent from 1 (t-test, n = 13, P < 0.006) and aerobicmineralisation is faster than anaerobic mineralisationat low mineralisation rates.

DISCUSSION

Methodological aspects

Before discussing the results and literature, it is in-structive to distinguish between experiments in whichthe entire sediment column is exposed directly to oxy-gen and experiments using sediment cores and manip-ulating the oxygen content of the overlying water. Inthe latter, only the top few millimetres of the sedimentare affected by the oxygen regime in the overlyingwater column, because oxygen typically becomes de-pleted within the upper 0 to 15 mm and most minerali-sation will occur anaerobically (apart from animal tubesetc. that may enable oxygen to protrude deeper into thesediment). The complete oxygenation/de-oxygenationof all depth strata in slurry incubations is comparable to

5

0- . 51(.2 4 0 0

..- . 51('

.Db ° FF

e 0..- 1 o OF

:I! 3 0'0) .. BG-B

0- - geometricmean

c:

Lb 0 rP 01110 - ':1 line

0(3:c 2

0E

eooB @D

E- 0.1QJ1111

DD

(J

0:c

0e

0800

Q)

(A)400 600

CO

0 200c:

lability of organic carbon

« 0.01

1 I(Jamof C g.1 TOC (1)

0.01 0.1

-..-b

..-'0)0(3EE- 0.1(J

:c0....Q)COc:« 0.01

Dauwe et al.: Effect of oxygen on degradation of organic matter 19

the 'thin layer technique' (e.g. Sun et at. 1993b), andenables us to assess the effect of oxygen on degradationindependently from oxygen diffusion.

Mineralisation rates based on slurry incubations maydeviate from iD sitll rates because slicing and homo-genisation of the sediment horizons may disturb micro-gradients of nutrients and enlarge the solid-liquid ratioso that micro-organisms have easier access to organicmatter (Aller & Aller 1998). However, studies of theeffects of slurry incubations on bacterial productionrates are not equivocal (Burdige 1989). The presenceof mineral surfaces may stimulate rates of incorpora-tion of organic substrates. even by 1 order of magni-tude in slurries (Meyer-ReilI986). or inhibit incorpora-tion rates compared to undisturbed sediments (Dobbset al. 1989), depending on the substrate. mineral andorganism involved.

Depth-integrated carbon dioxide production rangedfrom 12 to 140 mmol m-2 d-I (Fig. 4A) and covered thewhole range of mineralisation rates in estuarine andcoastal sediments (7 to 90 mmol m-z d-I: Heip et at.1995). A direct site-by-site comparison of available lit-erature data on oxygen uptake by North Sea sediments(Cramer 1990, van Raaphorst et at. 1992, Boon & Duine-veld 1998) with our integrated rates of carbon dioxideproduction is complicated by temperature differences.interannual and seasonal variability and the absence ofmacrofauna in our incubations (for details see Dauwe1999). However, during the sampling period, sedimentoxygen-uptake rates were measured at Stns Mol-2 andMol-3, being 175 :t 31 and 95 :t 4 mmol Oz m-z d-I, re-spectively. There is good agreement with carbon diox-ide production rates based on slurry incubations (141 :t9 and 99:t 19 mmol COz m-z d-I at Stns Mol-2 and Mol-3. respectively). Whatever bias there may be in ourslurry estimates relative to iD .mrrates, the comparativeaspect in terms of aerobic versus anaerobic mineralisa-tion is considered representative of natural sediment.

Aerobic versus anaerobic mineralisation

The results of this study indicate that differencesbetween aerobic and anaerobic mineralisation rates

are mainly related to the absolute rate (Figs. 4 & 5) andnot to the lability of the sedimentary organic matter(Fig. 6). Generally. the decay rate of sedimentaryorganic matter was rather similar in oxic and anoxicincubations (Figs. 3 & 5). In coarse-grained sedimentscharacterised by very low mineralisation rates (lessthan about 0.1 \lmol C g-I d-I ) such as those found atStns BF and BG-B. mineralisation rates under oxic con-

ditions were consistently and significantly higher thanthose under anoxic conditions at all investigateddepths (Fig. 3). The depth-consistent divergence in the

- - -

coarse-grained sediments is reflected by the signifi-cant deviation (t-test, n =51, P < 0.001) of the slope ofthe geometric mean regression line through the aero-bic versus the anaerobic mineralisation rate (slope =-1.41 :!:0.074) from the 1:1 line (Fig. SA). To ascertainthat oxygen did not become limiting at the end of theexperiment (the critical level is about 3 \lmol Oz I-I;GailIard & RabouilIe 1992), we included only sampleswith a final Oz concentration well above this level (con-taining >80 \lmol O2 I-I) in the geometric mean regres-sion. Inclusion of data points from stations for whichwe had no information on the final oxygen concen-tration (Stns BG-A, Mol-2, Mol-3, ZK) or from stationsat which the final oxygen concentration decreased to..., 15 \lmoU-1 (Stn GB) would not change the significantdeviation of the geometric mean regression (slope =1.24:t 0.054) from the 1:1 line (t-test. n = 120. P < 0.001).The ratio of aerobic versus anaerobic mineralisation

did not vary systematically over the broad range oforganic matter lability investigated in this study (about10 to >600 \lmol C g_1 TOC d-I: Fig. 6)..

The sediment dilution series incubations (Fig. 5B)provided additional support for a critical level of min-eralisation rather than organic matter lability control-ing the effect of oxygen on mineralisation rates. Themineralisation rate per unit weight varied, while thecomposition of the organic matter undergoing degra-dation remained constant. The slope of the geometricmean regression of the sediment dilution experiment(1.11:t 0.19) differed significantly from 1. and the pointof intersection with the 1:1 line (0.57 \lmol C g-I d-I:Fig. 5B) was comparable to that obtained in the cross- .system study (0.39 JImol C g-I d-I: Fig. 5A).

Our results seem to contrast with studies suggestingthat the lability of organic matter determines its sus-ceptibility to aerobic versus anaerobic decay. Usually,redox conditions are considered to have little influence

on the degradation rate of labile organic matter. suchas algae (Otsuki & Hanya 1972a,b), homogenised sed-

imentary organic matter (Kristensen & Blackbum1981), plankton material added to sediment cores(Westrich & Berner 1984, Henrichs & Reeburgh 1987,Lee 1992) or labile molecular compounds such as neu-tral sugars and amino acids (Hedges et at. 1988). Incontrast, oxic conditions have been reported to stimu-late degradation of more refractory organic material(Kristensen et at. 1995, Sun et at. 1997, Hulthe et at.

1998). Particularly aromatic structures and highly poly-meric compounds such as lignin have been found to bepoorly degradable under anoxic conditions (Benner etat. 1984). These specific differences in the degradabil-ity of terrestrial versus marine organic matter did notaffect the results of our study, since the main sourceof organic matter was marine phytoplankton for theNorth Sea stations (Dauwe & Middelburg 1998)and

- - -

'"

20 Mar Ecol Prog Ser 215: 13-22, 2001

estuarine phytoplankton and microphytobenthos forthe intertidal Molenplaat stations (Herman et al. 2000,Middelburg et a1. 2000).

The relatively low anaerobic mineralisation rates insediments with low amounts of degradable sedimen-tary carbon may indicate a critical activity limit belowwhich anaerobic bacterial communities operate lessefficiently than aerobic communities. We hypothesisethat (1) organic matter mineralisation at low ratesdepends on the bacterial biomass, and (2) that the oxy-gen effect at low rates can be attributed to a differencein growth or maintenance efficiency between aerobicand anaerobic bacteria. -

In order to better understand the link between min-eralisation level, bacterial biomasS and the effect of

oxygen on mineralisation, we have developed a sim-ple, generic model based on our hypothesis. Minerali-sation is a function of the quantity and quality of

organic matter (~J) and has a Monod-type depen-dence on the biomass of heterotrophic bacteria (B):

BM = I'(C)-

B+K.

where M is the mineralisation rate (~mol C g-I d-I),/'(C) is a function describing the dependence of miner-alisation rate on the quality and quantity of organicmatter substrate, B is the biomass of metabolicallyactive bacteria (~mol C g-I), and"is the Monod half-saturation constant for the influence of bacterial bio-

mass on mineralisation (~mol C g-I), The mineralisa-tion rate has a first-order dependence on bacterialbiomass at very low biomass, but a zero-order depen-dence at higher biomass values. This independence ofmineralisation from bacterial biomass at high biomassvalues is consistent with observations and theory(Boudreau 1992). The function f(C) does not have tobe specified for our purpose, but it probably can bedescribed by a first-order dependency on labile carbon(Westrich & Berner 1984, Middelburg 1989, Boudreau1992). Bacterial biomass evolves according to:

dB = '(.M-I.Bdt

where '( is metabolic efficiency (dimensionless), and I isthe biomass-specific loss rate (due to mortality andmaintenance respiration; d-I). When bacteria are as-sumed to be at steady state with the organic substrateavailable:

dB = 0dt

one obtains:

MI

I'(C)- - K.Y

Aerobic (Subscript 1) and anaerobic (Subscript 2)mineralisation are then given by:

lz1'(C)2- - Km

'(2

respectively.The model is generic, and study of its behaviour does

not require accurate knowledge of parameter values. Ifthe functional dependence of mineralisation of organicmatter does not depend on oxygen: i.e. /'(C)l = f(Clz,then M2 = MI-A, where

lz ItA = -KBZ--K.I and A< £(C)

'(2 '(I-

for physically real solutions.Anaerobic bacteria may have a lower metabolic effi-

ciency (y) and/or a higher biomass-specific loss rate, I(more biomass must be respired for the same energygain) than aerobic bacteria, and A is therefore positiveand finite. Model results for A > 0 clearly illustrate thataerobic mineralisation becomes faster than anaerobic

mineralisation at low activity levels (Fig. 5e). Adoptionof other values for A will change the actual values ofmineralisation but not the general appearance of themodel (Fig. Se): i.e. an oxygen effect at low minerali-sation rates, in agreement with our observations.

If the functional dependence of organic matter doesdepend on oxygen so that f(Clz = E.f(C)" then Mz =E.MI-A', where A' is a constant and Eis an efficiencyfactor (dimensionless). Such dependence on oxygenwould result in data parallel to the I: 1 line, but shiftedtowards lower values over the entire range (Fig. SC).Accordingly, it appears that the observed oxygeneffect is consistent with a model based on limitation of

mineralisation by bacterial biomass at low mineral-isation levels, and a differenC!e in growth and main-tenance efficiency of aerobic and anaerobic bacteria.

If our hypothesis of a 'criticallimit' of mineralisablecarbon needed to sustain anaerobic mineralisation is

valid, then the same stimulatory effect of oxygen ondegradation rate should be displayed not only by sedi.ments characterised by low amounts of labile organicmatter, as at Stns BF and BG-A, but also by sedimentscharacterised by large amounts of refractory organicmatter. The data on mineralisation rates at different

stations in the Skagerrak area (Hulthe et al. 1998) canbe used as an independent check. Hulthe et al. incu-bated surface and subsurface sediments for up to 60 dunder controlled oxic and anoxic conditions. Fig. SAshows that the mineralisation rates of their refractoryorganic matter falls in the same range of the labileorganic matter in our coarse-grained sediments at StnsBF and BG-B. Below about 0.1 ~mol C g-I d-I, bothsediment types showed consistently higher degrada-

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Dauwe et a!.: Effect of oxygen on degradation of organic matter 21

.tion rates under oxic conditions, regardless of their

contrasting lability: -1 to 23 ~mol C g -J TOC d- J at theSkagerrak stations of Hulthe et al. and about 100 to300 ~mol C g-l TOC d-J at Stns BF and BG-B.

A lower critical mineralisation level control of the

oxygen dependence of mineralisation is also consistentwith field observations. Enhanced oxidation arisingfrom downward progressing oxidation fronts has beenreported for deep-sea turbiditic (Wilson et al. 1985,Cowie et al. 1995) and sapropelic (pruysers et al. 1993)sediments with low mineralisation rates. Canfield

(1994) compiled evidence for enhanced preservationof organic matter in slowly accumulating sediments.Slowly accumulating (deep-sea) sediments are gener-ally also characterised by low mineralisation levels(Canfield 1994, ..Middelburg et al. 1997). The diver-gence of oxic and anoxic preservation occurs at anaccumulation rate in the order of 0.03 cm yr- J (Canfield1994), which represents a mineralisation rate in theorder of3 mmol m-z d-J or 0.02 ~mol C g-l d-J (usingdata compiled by Middelburg et al. 1997). This is con-sistent with a critical level of mineralisation as inferredfrom our cross-system and sediment dilution seriesincubations.

In conclusion, a cross-system analysis and sedimentdilution approach revealed that aerobic mineralisationof marine sedimentary material is faster at low miner-alisation levels, irrespective of the quality of organicmatter. The effect of oxygen on the degradation oforganic matter becomes apparent below a critical min-eralisation level at which bacterial biomass may limitmineralisation. Consistently, unequivocal field evi-dence for an oxygen effect has only been reported forslowly accumulating deep-sea sediments with lowmineralisation activities. Finally, our study has clearlydocumented that the effect of oxygen on mineralisa-tion depends not only on'the source, degradation stateand chemical composition of particulate organic matter(Benner et al. 1984, Canfield 1994. Kristensen et al.1995, Hulthe et al. 1998), but also on the mineralisationrate.

Acbow~ Pieter van Rijswijk, Adri Sandee andElfriede Burgers are gratefuIly acknowledged for their assis-tance with sediment sampling and with incubation experi-ments. Joop Nieuwenhuize, Bart Schaub and Yvonne Maasare thanked for their assistance with the GC measurements.The crews of RV 'Pelagia' and RV 'Luctor' are thanked fortheir support and pleasant stay during the cruise. Carlo Heipand the anonymous reviewers are gratefuIly acknowledgedfor criticaIly reading the manuscript. The research was finan-cially supported by the Netherlands Organisation for theAdvancement of Science (NWO), project VvA, under grant770-18-235 and the European Union ELOISE programme(projects ECOFLAT (ENV4-CT96-026) and PHASE (MAS3-CT96-0053». This is ELOlSE contribution 165 and publicationno. 2680 of the Netherlands Institute of Ecology.

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Submitted: December 6. 1999;Accepted: September 6. 2000Proofs received from author(s}:Apri/4. 2001

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