V ol. 215: 1 3 -2 2 ,2 0 0 1
MARINE ECOLOGY PROGRESS SERIES
M ar E col P rog Ser
P u b lish ed M ay 31
Effect of oxygen on the degradability of organic
matter in subtidal and intertidal sediments of
the North Sea area
Birgit Dauwe*, Jack J. Middelburg**, Peter M. J. Herman
N eth erlan d s Institute of E cology, K orrin gaw eg 7, 4401 N T Y ersek e, The N eth erlan d s
ABSTRACT: The effect of oxygen on the degradation of sedim entary organic m atter has b een d e te r­
m ined for 6 subtidal stations and 3 intertidal stations in the N orth Sea area. The stations w ere
selected to cover a ran g e of organic m atter lability and sedim ent texture (and hence concentrations
of organic m atter). Slurry incubations rev ealed th at at low m ineralisation rates, aerobic m ineralisa­
tion is significantly faster th a n anaerobic m ineralisation, irrespective of the d eg ree of lability of
organic m atter. A com plem entary incubation experim ent w ith sedim ent rich in organic carbon m ixed
w ith varying proportions of organically poor sedim ents confirm ed the en h an ced aerobic m ineralisa­
tion at low m ineralisation levels. It is proposed th at oxygen-enhanced degradation occurs at low m in­
eralisation levels at w hich bacterial biom ass production becom es limiting.
KEY WORDS: O rganic m atter • D egradation • O xygen • Sedim ents • N orth Sea • Intertidal
---------------------------------- Resale or republication not perm itted without written consent of the p ublisher---------------------------------
INTRODUCTION
In most coastal sedim ents, aerobic decom position is
lim ited to th e u p p er few m illim etres and to the walls
of ventilated anim al burrow s (Aller 1982), w hereas
anaerobic decom position is th e m ajor m ineralisation
process in th e d e e p e r layers of the sedim ent colum n
(Jorgensen 1983). The influence of sedim entary redox
conditions on m ineralisation rates is still a m atter of
debate. K now ledge of th e effect of oxygen on the
degradability of organic m atter is req u ired to b etter
define th e factors governing th e preservation of
organic m atter in m arine sedim ents (Canfield 1994,
H artnett et al. 1998, H ulthe et al. 1998). Decom position
of organic m atter is usually m odelled as having a firstorder or h igher-order (Westrich & B erner 1984, M id­
d elb u rg 1989) d e p en d en ce on organic m atter content,
in d ep en d en t of oxidant availability an d bacterial bio­
*P re se n t a d d ress: RIKZ, P o stb u s 8039, 4330 EA M id d e lb u rg ,
T h e N e th e rla n d s
" C o rre s p o n d in g author.
E-mail: m iddelburg@ cem o.nioo.knaw .nl
© In te r-R e se a rc h 2001
m ass (Boudreau 1999). If oxygen affects the d e g ra d ­
ability of organic m atter, this will require revision of
diagenetic models. M oreover, benthic anim als may
rapidly displace organic m aterial from the oxic to the
anoxic layers of sedim ents and vice versa (Aller 1994).
H ence, these organism s could thus affect the d e g ra d ­
ability of organic m atter (Aller & Aller 1998).
M uch effort has consequently b e en devoted to d e te r­
m ining w h eth er aerobic m ineralisation is faster than
anaerobic m ineralisation. Even though there is ex p eri­
m ental evidence th at m ineralisation rates of labile sed ­
im entary organic m atter are not significantly different
u n d er oxic and anoxic conditions (e.g. W estrich &
B erner 1984, Canfield 1989, Lee 1992, A ndersen 1996),
other studies have show n that some (refractory) com ­
pounds of the organic m atter d eg rad e m ore slowly
u n d er anoxic th an u n d er oxic conditions (H ansen &
B lackburn 1991, Sun et al. 1993a,b, Cowie et al. 1995,
H arvey et al. 1995, H ulthe et al. 1998). O ther ex p eri­
m ental studies have com e to the conclusion th at a n a e r­
obic processes m ay even be faster th a n aerobic p ro ­
cesses (e.g. K ristensen & B lackburn 1987, H ulthe et al.
1998). It has b een su ggested that the lability of organic
14
M ar Ecol Prog Ser 215: 13-22, 2001
m atter determ ines its relative susceptibility to aerobic
versus anaerobic decay (Hulthe et al. 1998), but also
source differences (even though they m ay be co­
related to quality) probably play a role (Benner et al.
1984, K ristensen et al. 1995).
G eoscientists have rep o rted field evidence of an
effect of oxygen on organic m atter d eg rad atio n on long
tim e scales. Wilson et al. (1985) o bserved that organic
m atter in a relict d ee p -se a turbidite from th e M adeira
abyssal plain exhibited little degrad atio n over a
140 000 yr period w h en exposed to sulphate, but that
80 % of the carbon w as resp ired w ithin 10 000 yr in the
presen ce of oxygen. Canfield (1994) p resen ted evi­
dence that preservation of organic m atter w as d e p e n d ­
ing on bottom -w ater oxygen concentrations at low,
but not at high, sedim ent accum ulation rates. M ore
recently, H artn ett et al. (1998) gave correlative evi­
dence that the period of tim e that organic m atter
is exposed to oxygen determ ines th e efficiency of
the m ineralisation processes. Sedim ent accum ulation
rates an d oxygen exposure tim es com prise m any
factors know n to affect m ineralisation on decadal and
m illennial tim e scales.
M ost experim ental results an d field studies support
the hypothesis that the quality of the organic m atter
controls w h eth er oxygen affects th e m ineralisation
process. However, sedim ents w ith m ore refractory
organic m atter show ing an o x ygen-dependent d e g ra d ­
ability usually also have low organic m atter co ncentra­
tions, w ith th e result th at m ineralisation rates are also
low. We hypothesise that th ere is a critical level of m in­
eralisation of organic m atter below w hich aerobic
degrad atio n is faster th an anaerobic degradation. In
m arine sedim ents, the concentration and lability of
organic m atter often co-vary because they both d e ­
crease upon degradation. To uncouple th e effect of
organic m atter lability and m ineralisation level from
the oxygen d e p en d en ce of m ineralisation, w e have
m ade a cross-system study in coastal sedim ents of the
N orth Sea area. Six subtidal stations and 3 intertidal
stations w ere selected to cover a range of organic m a t­
ter of various lability and sedim ent texture (and hence
concentrations of organic matter) (Dauwe & M iddel­
b u rg 1998, D auw e et al. 1999). M oreover, sedim ent
that w as rich in organic m atter from 1 intertidal site
w as m ixed w ith sedim ent of low organic m atter con­
tent to low er the m ineralisation level w hile m aintain­
ing the quality of the organic m atter constant.
MATERIALS AND METHODS
Sampling. Sedim ent sam ples w ere tak en from 6 su b ­
tidal stations in the N orth Sea in N ovem ber 1995
(Fig. 1, Table 1: Stns S kagerrak [SK], G erm an Bight
[GB], Friesian Front [FF], Broad Fourteens [BF]) and in
M ay 1996 (B rouw ershavensche-gat [Stns BG-A, BGB]). T hree intertidal stations w ere sam pled in Ju n e
1996, 2 located on a tidal flat in the W esterschelde
(M olenplaat: [Stns Mol-2 and Mol-3]) and 1 on a musselbank in the O osterschelde (Stn Z an dkreek [ZK])
(Fig. 1, Table 1). At the N orth Sea stations, most fresh
organic m atter originates from the deposition of p h y ­
toplankton blooms. The sedim entary organic m atter
reflects a broad sequence of different organic m atter
degradation states, probably due to ageing during la t­
eral bed-load transport w ith residual currents and dif­
ferences in w ater d ep th (Dauwe & M iddelburg 1998).
In the intertidal areas, fresh organic m atter input is
dom inated by prim ary production of benthic m icroalgae at Stns Mol-2 and Mol-3 (B arranguet et al. 1997)
and strong biodeposition of organic m atter as faeces on
T ab le 1. C h a rac te ristic s of s a m p lin g sta tio n s (lab e lle d as in Fig. 1) a n d c onditions of th e in c u b a tio n e x p e rim e n ts. V alu es in p a r e n ­
th e s e s a re for su rfa c e 0 to 1 cm la y e r of se d im e n t
Stn
L atitude
L ongitude
D epth
Sedim ent
(m) M edian TOC Sam pling
grain size (wt% ) period
(pm)
Incubation
period (d)
Oxic Anoxic
T
Gas
pH
TO
Oxic
Anoxic
Oxic
Anoxic
Subtidal
GB
SK
FF
BF
BG-A
BG-B
8° 09'
10° 15'
4o 30'
3o 52'
3°48'
3o 46'
E
E
E
E
E
E
54° 05'
58° 12'
53° 42'
53° 00'
51°45'
51°46'
N
N
N
N
N
N
20
270
39
28
5
3
(16)
(13)
(40)
(266)
(162)
(305)
31
12
83
248
185
354
1.12
2.47
0.51
0.05
0.16
0.02
Nov 95
Nov 95
Nov 95
Nov 95
M ay 96
M ay 96
21
19
20
22
27
27
22
20
21
22
27
27
16
16
16
16
16
16
n
2/ o 2
2/ o 2
n 2/ o 2
n 2/ o 2
n 2/ o 2
n 2/ o 2
n
n
n
2
2
n2
n2
n2
n2
6.9
6.6
7.1
7.0
6.9
7.0
(70) 120
(160) 180
(238) 190
0.52
0.18
0.25
Ju n 96
Ju n 96
Ju n 96
22
22
29
22
22
29
16
16
16
n
2/ o 2
2/ o 2
n 2/ o 2
n
n
n
± 0.3
± 0.3
± 0.05
± 0.15
±0.1
± 0.07
2
2
n2
6.9 ± 0.15
7.0 ±0.23
7.3 ± 0.08
7.1
7.3
7.2
7.1
7.3
7.3
±0.1
±0.1
±0.07
±0.04
± 0.24
±0.13
Intertidal
Mol-2
Mol-3
ZK
3o 5 7 '2 ' E
51° 2 6 '3 ' N
3o 5 6 '9 ' E 51° 26' 25' N
3o 5 4' E
51° 33' N
-
-
7.4 ±0.16
7.3 ±0.15
6.9 ±0.1
D auw e et al.: Effect of oxygen on d egradation of organic m atter
15
screw caps provided w ith ru b b er septa.
This resulted in a slurry:headspace ratio
60°
of 30:40 ml. H eadspaces w ere p u rg ed 3
tim es for 10 m in w ith N 2 for the anoxic
incubations and w ith N 2:0 2 (80:20) for
Norway
the oxic incubations. B etw een flushings,
the slurries w ere shaken and allow ed to
equilibrate for 10 min. Bottles containing
North S ea
only gas and bottles containing gas and
filtered seaw ater w ere used as controls.
Final changes in control flasks w ithout
sedim ent w ere always <3% of initial
concentrations. O ther controls contain­
ing sedim ent and w ater w ere poisoned
by adding 1 ml of 1 % HgCl. T here w as
The Netherlands
no significant C 0 2 release from poisoned
United Kingdom
sedim ents. CH4 release in the anoxic in ­
cubations w as maxim ally 2 % of C 0 2 re ­
lease, and w as therefore ignored. During
the w hole incubation period, the flasks
50°
w ere continuously rotated, allow ing an
optim al exchange b etw een the slurry
and the h eadspace gas (van der N at et
al. 1997). All slurries and controls w ere
incubated in the dark at 16°C for about
s a m p le s ta tio n s
20 to 30 d (Table 1). This length of in cu ­
resid u al tidal
cu rren ts
bation w as necessary to ensure sufficient
accuracy for low-activity sam ples. A se­
lection of sam ples covering the entire ac­
tivity range was incubated 10-fold un d er
Fig. 1. L ocations of sa m p lin g stations. (A) N o rth S ea stations: SK = S k a g e rra k ;
oxic and anoxic conditions to study the
GB = G e rm a n Bight; FF = F rie sian Front; BF = B ro ad F o u rte en s; BG = Broukinetics of degradation. C 0 2 production
w e rsh a v e n s c h e g a t A a n d B. (B) In te rtid a l stations: M ol = M o le n p la a t 2 a n d 3;
rates w ere linear for >40 d (Fig. 2), con­
ZK = Z a n d k re e k
sistent w ith observations by H ulthe et al.
(1998).
the sedim ents by m ussels at Stn ZK (H erm an et al.
H eadspace concentrations of C 0 2, 0 2 and CH4 w ere
determ ined using a Carlo Erba high-resolution MEGA
1999). Sam ples of the subtidal sedim ents w ere ob­
tain ed w ith a cylindrical R eineck-type box corer (31 cm
5340 gas chrom atograph, equipped w ith a flame ionii.d. [inner diam eter]), and subsam pled using acrylic
tubes (60 cm length, 3.3 cm i.d.). The intertidal Stns
Mol-2, Mol-3 and ZK w ere sam pled by direct coring
□ Oxic: R = 0.87
w ith acrylic tubes. At each station, 4 subcores w ere
■ Anoxic: R2 = 0.78
sliced and th en pooled p er depth stratum and then
m ixed. All m acrofauna and shell fragm ents w ere
rem oved prior to incubation. At Stns Mol-2 an d Mol-3,
replicate sedim ent oxygen-consum ption rates w ere
m easu red using a shipboard core-incubation tec h ­
nique (Moodley et al. 1998).
Degradability of organic matter. D egradability of or­
ganic m atter w as assessed by m easuring the production
20
30
of C 0 2 and CH 4, the end products of carbon m ineralisa­
Time
(d)
tion, in the head sp ace above sedim ent-w ater slurries. A
volum e of -2 0 ml sedim ent w as transferred into 70 ml
Fig. 2. E x am p le of th e e v o lu tio n of C 0 2 p ro d u c e d d u rin g a n
glass incubation bottles (Chrom pack), and diluted w ith
oxic a n d a n ano x ic in cu b a tio n . R e g ressio n lin e s a n d coeffi­
c ie n ts of d e te rm in a tio n a re sh o w n
10 ml filtered seaw ater; the bottles w ere sealed with
16
M ar Ecol Prog Ser 215: 13-22, 2001
SK
GB
FF
o. io
15
20
-
20
20
0
0.5
0
1
BF
0.5
0
1.5
1
0.2
BG-A
0.4
0.6
BG-B
E
o
15
20
15
-
20
20
0
0.05
0.1
0.15
.
0
0
3
2
1
0.05
Mol-3
Mol-2
+■*
a
a>
0.1
0.15
ZK
IQ-
10
-
15
15
-
■o
15
-
-
20
20
20
0
1
2
3
4
0
1
2
3
0
0.5
1
1.5
2
|jmol C g 1 d 1
Fig. 3. V e rtic al p rofiles of C 0 2 p ro d u c tio n p e r g d ry s e d im e n t a t sa m p lin g sta tio n s (lab e lle d as in Fig. 1). (□) O xic in cu b a tio n s;
(■) a noxie in c u b a tio n s
sation detector, a hot w ire detector, a m ethaniser and a
3 m H aysep-Q and 2 m m olsieve column. At the end of
the incubations, the vials w ere o pened and the pH w as
m easured. The sam ples w ere w eighed, freeze-dried,
and w eighed again in order to determ ine the dry
w eight and exact volum e of the incubated sedim ent.
The total am ount of gas p roduced or rem aining in
the incubation bottles w as calculated as the sum of the
head sp ace and dissolved concentrations. Equilibrium
concentrations of the gases in the sedim ent-w ater slur­
ries are based on m easured headspace concentrations
and tem perature- and salinity-dependent solubility
coefficients. For C 0 2, the pH -d ep en d en t spéciation
w as also tak en into account (Stumm & M organ 1996).
All m ineralisation rates w ere expressed as pmol C 0 2
(g dry sedim ent)-1 d-1, abbreviated as pmol C g-1 d-1.
Analytical reproducibility of total C 0 2 m easurem ents
is about 5 %, taking into account in h erent uncertainties
17
D auw e et al.: Effect of oxygen on deg rad atio n of organic m atter
in C 0 2 gas m easurem ents in the h ead space and in
slurry pH m easurem ents.
C 0 2 production generally resulted in some acidifi­
cation at the end of the experim ent during aerobic
m ineralisation com pared to the anoxic incubations
(Table 1), probably due to the buffering capacity of
m any of the anaerobic reaction products (e.g., H C 0 3~
H 2S and NH 4+) and sulphide oxidation in the oxic incu­
bations. The oxygen concentration in the oxic slurries
w as 234 pmol I-1 at the b eginning of the incubation and
15 to 80 pmol I-1 after 3 w k at the stations w ith high
m ineralisation rates (Stns SK and GB); this is well
above the 3 pmol I-1 w hich com prises the half-saturation constant for 0 2 lim itation in aerobic m ineralisation
(Gaillard & Rabouille 1992).
Preparation of sedim ent mixture. Surface sedim ent
(0 to 1 cm) w as collected at the intertidal Stn Mol-2 on
N ovem ber 23, 1998. The sedim ent w as freeze-dried
and diluted to 25, 6.25, 1.56 and 0.39% by adding an
organically poor sedim ent m ixture (0.03 wt%) of extra
pu re sand (Merck) and freeze-dried N orth Atlantic
deep -sea sedim ent (3:1). The sand:silt ratio of the
ad d ed m ixture w as similar to th at of the intertidal
sedim ent. These sedim ent m ixtures w ere incubated
as in the p reced in g subsection. Two replicates w ere
incubated for each of the 3 incubation periods (20, 23,
31 d).
Sedim ent parameters. Sedim ent param eters w ere
determ ined for a subsam ple of the initial sam ple.
M edian grain sizes w ere d eterm ined for freeze-dried
sam ples w ith a M alvern Particle Sizer 3600 EC. Poros­
ity w as calculated from w ater content (weight loss on
drying at 100°C) assum ing a dry density of 2.5 kg dm -3
for sedim ent. After in situ acidification w ith 25 % HC1
in p reclean ed silver cups to rem ove inorganic carbon
(N ieuw enhuize et al. 1994), organic carbon co ncentra­
tions w ere d eterm ined as total carbon.
Vertical profiles m easured u n der oxic and anoxic
conditions had similar shapes at most stations (Fig. 3),
except at Stn BF w here the aerobic profile show ed an
extended subsurface peak, w hereas the anaerobic p ro ­
file rem ained constant w ith depth. The consistent dif­
ferences betw een carbon dioxide production u n der
oxic and anoxic conditions over the entire sedim ent
d epth (Fig. 3) w ere reflected by the ratio of aerobic
versus anaerobic m ineralisation rates based on depthintegrated C 0 2 production (Fig. 4B). The aerobic m in­
eralisation rate w as significantly higher th an the
anaerobic 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) sedim ents, w ith ratios of aerobic rate versus
anaerobic rate of b etw een 1.7 and 2.7. At the other sta­
tions, aerobic and anaerobic m ineralisation rates w ere
similar (Stns GB, BG-A, Mol-2, Mol-3) or anaerobic
rates w ere 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 m inerali­
sation rate is given for all sedim ents th at had an oxy­
gen concentration of m ore th an 80 pmol 0 2 I-1 at the
end of the oxic incubations (Fig. 5A). The slope of the
geom etric m ean regression line (1.41 ± 0.074) is signif­
icantly different from 1 (Student's f-test, n = 57, p <
0.001), indicating that m ineralisation rates of sedim en­
tary organic m atter are different u n d er anoxic com ­
p ared to oxic conditions. A lthough the differences at
interm ediate to high m ineralisation rates w ere mar-
intertidal
125
100
-
75
o
50
-
25
-
nA
TD
c
o
RESULTS
At most stations, carbon dioxide production
decreased strongly w ith increasing depth, except at
Stn BF (Fig. 3). Very steep profiles w ere found at the
intertidal Stns Mol-2, Mol-3 and ZK (>90% d ecrease
w ith respect to surface m ineralisation), w hereas the
rates at Stns SK, FF, BG-A and BG-B d ecreased m ore
gradually (60 to 75% of original surface concentration
at 5 cm depth). At Stn GB, d eg rad ab le carbon initially
increased w ith increasing d ep th and th en decreased
(Fig. 3B). D epth-integrated (0 to 15 cm) carbon dioxide
production, b ased on the av erage of oxic and anoxic
incubation, varied from 12 to 140 mmol m-2 d-1
(Fig. 4A); the seq uence was: Mol-2 > ZK = GB = Mol-3
> BG-A > SK = FF > BG-B = BF.
subtidal
(A)
150
GB
_È_
SK
BF
JÜL
BG-A
BG-B
Mol-2
subtidal
(B)
M ol-3
ZK
intertidal
O 3i
O
JD
0) o
03
¿
C
il
03
Ü
1
o
□ □
CD
03
o
GB
SK
FF
BF
Fig. 4. (A) D e p th -in te g ra te d
d u c tio n (x ± SD a e ro b ic
(B) ratio of d e p th -in te g ra te d
alisation. S a m p lin g statio n s
BG-A
BG-B
Mol-2
M ol-3
ZK
(0 to 15 cm) c a rb o n dio x id e p r o ­
a n d a n a e ro b ic m ineralisatio n );
a e ro b ic v e rsu s a n a e ro b ic m in e r­
(abscissas) la b e lle d as in Fig. 1
18
M ar Ecol Prog Ser 215: 13-22, 2001
o2
!q
O)
O
ö
A
4
o
BG -B
0
CO
geometric mean
1:1 line
C
05
Ö
E
zL
o
2
-
0
0
□A
I
0
CO
C
<C
0.01
-
200
0.01
•
O
■
0.1
1
A
0.39%
geometric mean
1:1 line
E
0.1
o
io
oV—
0
0
c
<
0.01
0.01
—
D)
O
ö
0.1
1
1:1 line (E=A=1)
A = 0.03; E = 1
A = 0.01; E = 1
A = 0.03; E = 0.5
E
o
0.1
'jd
o
0
0
C
<
600
800
Lability of organic carbon
(pmol C g'1 TOC d'1)
Fig. 6. Ratio b e tw e e n m e a s u re d a e ro b ic a n d a n a e ro b ic m in e r­
a lisa tio n ra te s as a fu n c tio n of th e lab ility of o rg a n ic c arb o n
(d e fin e d as th e m in e ra lisa tio n ra te d iv id e d b y th e o rg a n ic c a r­
b o n c o n te n t of th e se d im e n ta ry o rg a n ic m atter). TO C: to ta l
o rg a n ic c arb o n
100 %
25%
6.25%
1
O)
O
ö
400
To investigate w h ether the observed differences b e ­
tw een aerobic and anaerobic mineralisation rates cor­
related with the lability of the organic matter, the ratio of
aerobic versus anaerobic rate w as plotted against the
lability of the organic m atter expressed as the am ount of
carbon m ineralised per gram total organic carbon (TOC)
per day (Fig. 6). There was no clear trend in the ratio over
the large range of lability m easured for sedim entary
organic m atter (-10 to >600 pmol C g_1 TOC d_1).
During incubation of the sedim ent dilution series,
dissolved oxygen concentrations w ere alw ays above
140 pM. Fig. 5B shows the log-log plot of aerobic v er­
sus anaerobic degradation. Again, the slope of the g eo ­
m etric m ean regression (1.77 ± 0.19) is significantly
different from 1 (t-test, n = 13, p < 0.006) and aerobic
m ineralisation is faster th an anaerobic m ineralisation
at low m ineralisation rates.
0.01
DISCUSSION
Aerobic (pmol C g -1 d"1)
Fig. 5. L og-log plots of a e ro b ic v e rsu s a n a e ro b ic m in e ra lisa ­
tio n ra te s. (A) S e d im e n ta ry o rg a n ic m a tte r from Stns SK, FF,
BF a n d BG-B, a t all d e p th in te rv a ls (SK*: d a ta from H u lth e et
al. [1998]: se e 'D iscussion'), sh o w in g 1:1 a n d g e o m e tric m e a n
re g re ss io n lines; (B) d ilu tio n e x p e rim e n t w ith p e r c e n ta g e of
o rig in a l se d im e n t, sh o w in g 1:1 a n d g e o m e tric m e a n r e g r e s ­
sion lines; (C) m o d el re su lts for A = 0.03, E = 1; A = 0.01, E = 1;
a n d A = 0.03, E = 0.5 (A = con stan t; E = efficiency factor)
ginal, at low m ineralisation rates (<0.1 pm ol C g -1 d-1),
typical for the sandy Stns BF and BG-B (Fig. 5A), a ero ­
bic m ineralisation w as up to 50% hig h er th an rates
m easu red u n d er anoxic conditions.
M ethodological aspects
Before discussing the results and literature, it is in ­
structive to distinguish b etw een experim ents in w hich
the entire sedim ent colum n is exposed directly to oxy­
gen and experim ents using sedim ent cores and m anip­
ulating the oxygen content of the overlying w ater. In
the latter, only the top few m illim etres of the sedim ent
are affected by the oxygen regim e in the overlying
w ater column, because oxygen typically becom es d e ­
pleted w ithin the up p er 0 to 15 mm and most m inerali­
sation will occur anaerobically (apart from anim al tubes
etc. that m ay enable oxygen to protrude deep er into the
sedim ent). The com plete oxygenation/de-oxygenation
of all depth strata in slurry incubations is com parable to
D auw e et al.: Effect of oxygen on degrad atio n of organic m atter
the 'thin layer tech n iq u e' (e.g. Sun et al. 1993b), and
enables us to assess th e effect of oxygen on degradation
indep en d en tly from oxygen diffusion.
M ineralisation rates b ased on slurry incubations m ay
deviate from in situ rates becau se slicing and hom o­
genisation of the sedim ent horizons m ay disturb m icro­
gradients of nutrients an d en larg e the solid-liquid ratio
so that m icro-organism s have easier access to organic
m atter (Aller & Aller 1998). However, studies of the
effects of slurry incubations on bacterial production
rates are not equivocal (Burdige 1989). The presence
of m ineral surfaces m ay stim ulate rates of incorpora­
tion of organic substrates, ev en by 1 order of m ag n i­
tude in slurries (M eyer-Reil 1986), or inhibit incorpora­
tion rates com pared to u n d istu rb ed sedim ents (Dobbs
et al. 1989), d ep en d in g on the substrate, m ineral and
organism involved.
D epth-integrated carbon dioxide production ran g ed
from 12 to 140 mmol n r 2 d_1 (Fig. 4A) an d covered the
w hole ran g e of m ineralisation rates in estu arine and
coastal sedim ents (7 to 90 mmol n r 2 d-1: H eip et al.
1995). A direct site-by-site com parison of available lit­
eratu re d ata on oxygen up tak e by N orth Sea sedim ents
(Cram er 1990, v an Raaphorst et al. 1992, Boon & Duineveld 1998) w ith our in teg rated rates of carbon dioxide
production is com plicated by tem p eratu re differences,
interan n u al and seasonal variability and the absence of
m acrofauna in our incubations (for details see D auw e
1999). However, durin g the sam pling period, sedim ent
oxygen-uptake rates w ere m easu red at Stns Mol-2 and
Mol-3, b ein g 175 ± 37 an d 95 ± 4 mmol 0 2 n r 2 d-1, re ­
spectively. T here is good ag reem en t w ith carbon diox­
ide production rates b ased on slurry incubations (141 ±
9 an d 99 ± 19 mmol C 0 2 n r 2 d_1 at Stns Mol-2 and Mol3, respectively). W hatever bias th ere m ay be in our
slurry estim ates relative to in situ rates, the com parative
aspect in term s of aerobic versus anaerobic m ineralisa­
tion is considered rep resen tativ e of natu ral sedim ent.
A erobic versus anaerobic mineralisation
The results of this study indicate that differences
betw een aerobic an d anaerobic m ineralisation rates
are m ainly related to th e absolute rate (Figs. 4 & 5) and
not to the lability of th e sedim entary organic m atter
(Fig. 6). Generally, the decay rate of sedim entary
organic m atter w as rath er similar in oxic an d anoxic
incubations (Figs. 3 & 5). In coarse-grained sedim ents
ch aracterised by very low m ineralisation rates (less
th an about 0.1 pm ol C g-1 d-1 ) such as those found at
Stns BF and BG-B, m ineralisation rates u n d er oxic con­
ditions w ere consistently an d significantly h ig her th an
those u n d er anoxic conditions at all investigated
dep th s (Fig. 3). The depth-consistent d ivergence in the
19
coarse-grained sedim ents is reflected by the signifi­
cant deviation (f-test, n = 57, p < 0.001) of the slope of
the geom etric m ean regression line through the ae ro ­
bic versus the anaerobic m ineralisation rate (slope =
1.41 ± 0.074) from the 1:1 line (Fig. 5A). To ascertain
that oxygen did not becom e lim iting at the en d of the
experim ent (the critical level is about 3 pmol 0 2 F 1:
G aillard & Rabouille 1992), w e included only sam ples
w ith a final 0 2 concentration w ell above this level (con­
taining >80 pmol 0 2 F 1) in the geom etric m ean re g re s­
sion. Inclusion of d ata points from stations for w hich
w e h ad no inform ation on the final oxygen concen­
tration (Stns BG-A, Mol-2, Mol-3, ZK) or from stations
at w hich the final oxygen concentration decreased to
-15 pmol F 1 (Stn GB) w ould not change the significant
deviation of the geom etric m ean regression (slope =
1.24 ± 0.054) from the 1:1 line (f-test, n = 120, p < 0.001).
The ratio of aerobic versus anaerobic m ineralisation
did not vary system atically over the broad range of
organic m atter lability investigated in this study (about
10 to >600 pmol C g -1 TOC d -1: Fig. 6).
The sedim ent dilution series incubations (Fig. 5B)
provided additional support for a critical level of m in­
eralisation rath er th an organic m atter lability controling the effect of oxygen on m ineralisation rates. The
m ineralisation rate p er unit w eight varied, w hile the
com position of the organic m atter undergoing d e g ra ­
dation rem ained constant. The slope of the geom etric
m ean regression of the sedim ent dilution experim ent
(1.77 ± 0.19) differed significantly from 1, and the point
of intersection w ith the 1:1 line (0.57 pmol C g-1 d-1:
Fig. 5B) w as com parable to th at obtained in the cross­
system study (0.39 pmol C g-1 d_1: Fig. 5A).
O ur results seem to contrast w ith studies suggesting
that the lability of organic m atter determ ines its sus­
ceptibility to aerobic versus anaerobic decay. Usually,
redox conditions are considered to have little influence
on the degradation rate of labile organic m atter, such
as algae (Otsuki & H anya 1972a,b), hom ogenised se d ­
im entary organic m atter (Kristensen & Blackburn
1987), plankton m aterial ad d ed to sedim ent cores
(Westrich & B erner 1984, H enrichs & R eeburgh 1987,
Lee 1992) or labile m olecular com pounds such as n e u ­
tral sugars and amino acids (H edges et al. 1988). In
contrast, oxic conditions have b een rep o rted to stim u­
late degradation of m ore refractory organic m aterial
(Kristensen et al. 1995, Sun et al. 1997, H ulthe et al.
1998). Particularly arom atic structures and highly poly­
meric com pounds such as lignin have b ee n found to be
poorly deg rad ab le u n d e r anoxic conditions (Benner et
al. 1984). These specific differences in the d eg ra d ab il­
ity of terrestrial versus m arine organic m atter did not
affect the results of our study, since the m ain source
of organic m atter w as m arine phytoplankton for the
N orth Sea stations (Dauwe & M iddelburg 1998) and
20
M ar Ecol Prog Ser 215: 13-22, 2001
estuarine phytoplankton an d m icrophytobenthos for
the intertidal M olenplaat stations (H erm an et al. 2000,
M iddelburg et al. 2000).
Aerobic (Subscript 1) and anaerobic (Subscript 2)
m ineralisation are th en given by:
M1 =
The relatively low anaerobic m ineralisation rates in
sedim ents w ith low am ounts of d eg rad ab le sedim en­
tary carbon m ay indicate a critical activity limit below
w hich anaerobic bacterial com m unities operate less
efficiently th a n aerobic com m unities. We hypothesise
that (1) organic m atter m ineralisation at low rates
d ep en d s on th e bacterial biom ass, an d (2) that the oxy­
gen effect at low rates can be attrib u ted to a difference
in grow th or m aintenance efficiency b etw een aerobic
and anaerobic bacteria.
In order to b etter u n d erstan d th e link b etw een m in­
eralisation level, bacterial biom ass and th e effect of
oxygen on m ineralisation, w e have developed a sim ­
ple, generic m odel b ased on our hypothesis. M inerali­
sation is a function of th e quantity and quality of
organic m atter (f(C)J and has a M onod-type d e p e n ­
dence on th e biom ass of heterotrophic b acteria (B):
M = /(C )— - —
B +K b
w h ere M is the m ineralisation rate (pmol C g-1 d-1),
i(C) is a function describing the d e p en d en ce of m iner­
alisation rate on the quality an d q uantity of organic
m atter substrate, B is the biom ass of m etabolically
active bacteria (pmol C g-1), an d KB is th e M onod half­
saturation constant for the influence of bacterial bio­
m ass on m ineralisation (pmol C g-1). The m ineralisa­
tion rate has a first-order d e p en d en ce on bacterial
biom ass at very low biom ass, but a zero-order d e p e n ­
dence at h ig h er biom ass values. This in d ep en d en ce of
m ineralisation from bacterial biom ass at high biom ass
values is consistent w ith observations and theory
(Boudreau 1992). The function f(C) does not have to
be specified for our purpose, but it probably can be
described by a first-order d ep en d en cy on labile carbon
(Westrich & B erner 1984, M iddelburg 1989, Boudreau
1992). Bacterial biom ass evolves according to:
—
df
= J-M-1B
w h ere y is m etabolic efficiency (dimensionless), and 1 is
the biom ass-specific loss rate (due to m ortality and
m aintenance respiration; d_1). W hen b acteria are a s­
sum ed to be at steady state w ith the organic substrate
available:
dB
= 0
df
one obtains:
M = í ( C ) - —K b
Y
and
M 2 = f(C)2 - ^ - K B
Yi
Y2
respectively.
The m odel is generic, and study of its behaviour does
not require accurate know ledge of param eter values. If
the functional d e p en d en ce of m ineralisation of organic
m atter does not d ep e n d on oxygen: i.e. f(C)1 = f(C)2,
th en M 2 = M t - A , w here
A = — K B2- — K B1
Y2
and A < f ( C )
Yi
for physically real solutions.
A naerobic bacteria m ay have a low er m etabolic effi­
ciency (y) and/or a higher biom ass-specific loss rate, 1
(more biom ass m ust be respired for the sam e energy
gain) th a n aerobic bacteria, and A is therefore positive
and finite. M odel results for A > 0 clearly illustrate that
aerobic m ineralisation becom es faster th an anaerobic
m ineralisation at low activity levels (Fig. 5C). A doption
of other values for A will change the actual values of
m ineralisation but not the g en eral ap p earance of the
m odel (Fig. 5C): i.e. an oxygen effect at low m inerali­
sation rates, in ag reem ent w ith our observations.
If the functional depen d en ce of organic m atter does
dep en d on oxygen so th at f(C)2 = E-f(C)t , th en M2 =
E - M ^ A ' , w h ere A' is a constant and E is an efficiency
factor (dimensionless). Such depen d en ce on oxygen
w ould result in d ata parallel to the 1:1 line, but shifted
tow ards low er values over the entire range (Fig. 5C).
Accordingly, it appears that the observed oxygen
effect is consistent w ith a m odel b ased on lim itation of
m ineralisation by bacterial biom ass at low m ineral­
isation levels, and a difference in grow th and m ain­
tenance efficiency of aerobic and anaerobic bacteria.
If our hypothesis of a 'critical limit' of m ineralisable
carbon n eed ed to sustain anaerobic m ineralisation is
valid, th en the sam e stim ulatory effect of oxygen on
degradation rate should be displayed not only by sedi­
m ents characterised by low am ounts of labile organic
m atter, as at Stns BF and BG-A, but also by sedim ents
characterised by large am ounts of refractory organic
m atter. The d a ta on m ineralisation rates at different
stations in the S k agerrak area (Hulthe et al. 1998) can
be used as an in d ep en d en t check. H ulthe et al. in cu ­
b ated surface and subsurface sedim ents for up to 60 d
u n d er controlled oxic and anoxic conditions. Fig. 5A
shows th at the m ineralisation rates of their refractory
organic m atter falls in the sam e range of the labile
organic m atter in our coarse-grained sedim ents at Stns
BF and BG-B. Below about 0.1 pmol C g-1 d_1, both
sedim ent types show ed consistently higher degrada-
D auw e et al.: Effect of oxygen on degrad atio n of organic m atter
tion rates u n d er oxic conditions, regard less of their
contrasting lability: ~1 to 23 pm ol C g -1 TOC d_1 at the
Skag errak stations of H ulthe et al. an d about 100 to
300 pm ol C g -1 TOC d -1 at Stns BF an d BG-B.
A low er critical m ineralisation level control of the
oxygen d e p en d en ce of m ineralisation is also consistent
w ith field observations. E nhanced oxidation arising
from dow nw ard p rogressing oxidation fronts has b een
rep o rted for d eep -sea turbiditic (Wilson et al. 1985,
Cowie et al. 1995) an d sapropelic (Pruysers et al. 1993)
sedim ents w ith low m ineralisation rates. Canfield
(1994) com piled evidence for e n h an ced preservation
of organic m atter in slowly accum ulating sedim ents.
Slowly accum ulating (deep-sea) sedim ents are g e n e r­
ally also ch aracterised by low m ineralisation levels
(Canfield 1994, M iddelburg et al. 1997). The diver­
gence of oxic an d anoxic p reservation occurs at an
accum ulation rate in the order of 0.03 cm y r-1 (Canfield
1994), w hich rep resen ts a m ineralisation rate in the
order of 3 mmol n r 2 d_1 or 0.02 pm ol C g-1 d_1 (using
d ata com piled by M iddelburg et al. 1997). This is con­
sistent w ith a critical level of m ineralisation as inferred
from our cross-system an d sedim ent dilution series
incubations.
In conclusion, a cross-system analysis an d sedim ent
dilution approach rev ealed th at aerobic m ineralisation
of m arine sedim entary m aterial is faster at low m iner­
alisation levels, irrespective of the quality of organic
m atter. The effect of oxygen on the d eg rad ation of
organic m atter becom es a p p aren t below a critical m in­
eralisation level at w hich bacterial biom ass m ay limit
m ineralisation. Consistently, unequivocal field evi­
dence for an oxygen effect has only b e e n rep o rted for
slowly accum ulating d ee p -se a sedim ents w ith low
m ineralisation activities. Finally, our study has clearly
docum ented that the effect of oxygen on m ineralisa­
tion d ep en d s not only on the source, d eg rad ation state
an d chem ical com position of particulate organic m atter
(Benner et al. 1984, Canfield 1994, K ristensen et al.
1995, H ulthe et al. 1998), but also on the m ineralisation
rate.
A c k n o w le d g e m e n ts . P ie te r v a n R ijsw ijk, A d ri S a n d e e a n d
E lfried e B u rg e rs a re g ra te fu lly a c k n o w le d g e d for th e ir a ssis­
ta n c e w ith s e d im e n t sa m p lin g a n d w ith in c u b a tio n e x p e ri­
m en ts. Jo o p N ie u w e n h u iz e , B art S c h a u b a n d Y vonne M a a s
a re th a n k e d for th e ir a ssista n c e w ith th e G C m e a su re m e n ts.
T h e c rew s of RV 'P e la g ia ' a n d RV 'L uctor' a re th a n k e d for
th e ir s u p p o rt a n d p le a s a n t sta y d u rin g th e cruise. C arlo H e ip
a n d th e a n o n y m o u s re v ie w e rs a re g ra te fu lly a c k n o w le d g e d
for critically re a d in g th e m a n u sc rip t. T h e re s e a rc h w a s f in a n ­
cially s u p p o rte d b y th e N e th e rla n d s O rg a n isa tio n for th e
A d v a n c e m e n t of S c ien c e (NW O), p ro je c t VvA, u n d e r g ra n t
770-18-235 a n d th e E u ro p e a n U n io n ELO ISE p ro g ra m m e
(projects E C O FL A T (E N V 4-C T 96-026) a n d PH A SE (MAS3CT96-0053)). T his is ELOISE c o n trib u tio n 165 a n d p u b lic a tio n
no. 2680 of th e N e th e rla n d s In stitu te of Ecology.
21
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Editorial responsibility: Otto K inne (Editor),
O ldendorf/Luhe, G erm any
Subm itted: D ecem ber 6, 1999: A ccepted: S e p te m b e r 6, 2000
Proofs received from author(s): A pril 4, 2001