BLACKBURN, T. H., AND K. HENRIKSEN. Nitrogen cycling in

Limnol. Oceanogr., 28(3), 1983, 477493
@ 1983, by the American
Society
of Limnology
and Oceanography,
Nitrogen cycling in different
from Danish waters1
T. H. Bluckburn
und K. Henriksen2
Institute
and Genetics,
for Ecology
University
Inc.
types of sediments
of Aarhus,
DK 8000 Aarhus
C, Denmark
Abstract
Variations in sediment N:C ratios were correlated with water depth and season. 15NH,+ was
used to measure the rates of NH,+ production
(d) and incorporation
into bacterial cells (i) in
sediments from different stations, at different
seasons. The validity of the rates d and i was
indicated by the predicted correlation
of cl:i ratios with N:C ratios of the sediment, and the
predicted N:C ratio at which net NH4+ uptake occurred. There was also a correlation between
rate cl and product (total NH,+). In the O-2-cm stratum correlations
were also established
between d, exchangeable NH4+ pool, ratio exchangeable
NH?+ : porewater NH4+, flux of NH,+
from sediment, and flux of NH4+ into exchangeable
pool. The NO:,- flux from sediment was
correlated with nitrification
rate and with season. Benthic infauna increased the flux of NHI’
from the sediment by 50%. The rates of transfer of nitrogen (NO,-, NH?+, N,) from sediment
to water were 44-66% of the net rates of organic nitrogen mineralization
(d - i). Flux of
NO,- + NII,+ from the sediment could supply 30-82% of the nitrogen requirement
of the
planktonic primary producers.
Available nitrogen occurs in sediment
in the following
major pools: organic N,
porewater
ammonium
(NH,+pw),
exchangeable
ammonium
( NH4+ex), dissolved nitrate, and nitrogen gas. Our objective here was to measure these pools
and the rates that connect them to each
other and to the overlying water.
The rate of organic-N mineralization,
equivalent to the rate of NH,+ production
(d), and the rate of NH,+ incorporation
into cells (i), was measured by lsNH4+ dilution. Factors affecting the sediment organic N:C ratio, and the effect of the N:
C ratio on the ratio d:i were investigated.
The NH,+ that was not incorporated
into cells (net ammonium production,
d i) had three possible fates. Some passed
from the sediment to the overlying water,
some was oxidized to nitrate, and the rest
entered the sediment NH4+ pool. We examined the factors, mainly the ratio of
NH4+ex : NH,+pw in the 0-2-cm stratum,
which regulated the fate of NH,+. We also
examined
the factors, mainly seasonal
changes, which regulated the loss of NO,-
’ This work was supported
by grants from the
Danish Natural Science Council.
’ Present address: Botanical Institute, University
of Aarhus, Nordlandsvej
68, DK 8240 Risskov, Dcnmark.
to either the overlying water or to denitrification.
The total flux of nitrogen from
sediment to water (NH4+, N03-, N2) was
compared with net ammonium
production (d - i), and the contribution
of
NH,+ + NO,- to the pelagic primary producers was assessed.
We have placed considerable emphasis
on looking at correlations between pools
and rates and on trying to fit them into an
integrated model. We think that this is a
reliable method for cross-checking
the
validity
of the measurements.
The data
used here were collected from 11 stations
in Danish coastal waters.
We thank K. Maagaard and B. M. Pedersen for technical assistance.
Materials und methods
Sediment samples were taken during
two cruises of RV Martin Knudsen in November 1978 and July 1979. The stations
were in one of four groups (Fig. 1): the
Belt Sea group (sta. 2,3), the western Kattegat group (sta. 5, 8, 13, 14), the eastern
Kattegat group (sta. 6,9, lo), and the Skagerrak group (sta. 11, 12). The sediment
was collected with a “Haps” coring cylinder (Kanneworf
and Nicolaisen
1973).
Subcores were taken in various sizes of
Plexiglas tubes and were used in the following procedures.
Sediment composition--Specific
grav-
477
478
Blackburn
and Henriksen
9*
56O
55O
Fig. 1. Locations of stations in the Belt Sea (2,
3), Skagerrak (11, 12), eastern Kattegat (6,9, lo), and
western Kattegat (5, 8, 13, 14). Sediment type: stippled-sand;
horizontal
ruled-sandy
mud; vertical
ruled-mud;
solid-mud
with high organic content.
ity and water content were measured in
duplicate in known volumes of sediment
from each station that were weighed,
dried at 105°C for 24 h, and then reweighed. All rates and concentrations
are
expressed per cm3 of wet sediment. Organic content was measured by weight
loss at 450°C. The C, H, and N composition of the sediment organic matter was
determined in duplicate, on two replicate
samples, with a Hewlett-Packard
CHN
analyzer (model 185B CHN analyzer and
3380A integrator). Porewater and KC1 extracts (10 g of sediment + 10 ml of 1 M
KCl, 0.5 h at room temp) were obtained
by centrifugation
at 2,000 x g for 10 min
(Henriksen et al. 1981). The sediment was
from five pooled cores, sliced at intervals.
The KCl-extractable
NH4+ was defined as
total ammonium; this value minus porewater NH,+pw was defined as exchangeable NH4+ex.
Chemical
analyses-NH4+,
NO,- +
NOz-, and POd3- were measured onboard
by autoanalyzer (Chemlab Instr. Ltd., Essex) using the methods
of Solorzano
(1969), Armstrong et al. (1967), and Chan
and Kiley (1970).
Rate measurements-Rates
of NH,+
production
(d) and uptake (i) were measured using a 15NH,+ dilution technique
in a mixed sediment, incubated anaerobically (Blackburn
197%). In addition, d
was measured in July by injecting 15NH,+
into intact sediment cores from which the
surface water had been drained.
The
15NH,+ tracer (50 ~1 of sterile seawater
containing
500 nmol, 99% rsNHq+) was
injected into six cores with silicone rubber injection ports (Jergensen 1977). The
cores were incubated in the dark at the
sediment temperature;
three were fractionated at 1 day and the other three after
2 days. Each fraction was extracted with
10 ml of 1 M KC1 for 0.5 h at ambient
temperature.
The sediment + KC1 was
centrifuged
at 2,000 x g for 10 min and
the KC1 extract frozen until analysis for
NH,+ and l”N content (Blackburn 1979u).
With the mixing technique
(Blackburn
I979u) the correlation coefficients for the
slopes d - i (NH,+ vs. time) and -dl(d i) were >0.95 in the upper 8 cm where
these rates were high; correlation coefficients were often lower below 8 cm where
NH,+ concentrations
and 15N content did
not vary significantly
with length of incubation.
The rates in replicate
cores
could vary by 50%, as previously
noted
(Blackburn
1979a). With the injection
technique, d could be calculated by two
different
procedures.
In neither procedure did we use the model of Blackburn
(I979u) as there was no significant change
in ammonium concentration.
In the first
procedure,
we calculated
the rate constant k(day-I):
k = (ln15No - ln15Nt)/t
excess
(where 15N0 was the calculated
percentage of 15NH,+ at time 0, and 15Nt
was the measured excess percentage of
15N after t days of incubation).
We calculated the rate of ammonium production
d as
d = k x measured
NH,+ concentration.
Sediment
Rate
cm
Sta.2
Fig. 2.
procedure
nitrogen
of N Hi production
(n mol crfi3daf1 )
Sta.6
479
cycle
(d >
Sta.8
Rates of NH4+ production
measured by 15N dilution
with
vs. sediment depth. Results are for July at four stations.
The mean of the six d values for each
depth was calculated.
Generally
these
values had a standard deviation of ~50%.
In the second procedure, we calculated
the rate constant IE:
& = (lnYV,
- ln1.5N,)lt
(where 15N1 and 15N2 were the means of
the excess percentage of 15NH,+ for sections of three cores, measured after 1 and
2 days of incubation).
d = k x mean NH4+ concentration
for six cores.
The values of d by the first procedure
were lo-20% higher than by the second
procedure, probably due to adsorption of
15NHq+. We used the lower values.
Rates of NH,+ oxidation (nitrification)
in these sediments were also measured;
most of the results were given elsewhere
(Henriksen
et al. 1981). Some porewater
and total NIL+ profiles, NO,- profiles, and
flux of NO,- to the overlying water from
these sediments were also reported by
Henriksen et al. (1981).
Fluxes of NH J+, N03-, and POd3- were
measured in short incubations (8 h) in 10
undisturbed
cores (2.6-cm diam), with
gentle stirring of the water to maintain in
situ gradients of oxygen in the sediment
surface layer (Jorgensen 1977). The water
column of each core was replaced with
Sta. 5
a mixed
(0) and an injection
(Cl)
bottom water from the same station before incubation.
Concentrations
of N03-,
NH 4+, and PO,“- d uring the incubation
were measured. Cores containing
larger
macrofauna were omitted from flux calculations.
Four Haps cores (0.017 m2) from 0- to
20-cm depth from each station were analyzed for infauna. The large species were
picked by hand and the sediment was
then washed through a 2-mm sieve. We
determined
excretion rates of NH,+ and
POd3- from undamaged
animals of the
quantitatively
most important species by
incubating them in bottom water from the
sampling
station at ambient
sediment
temperature
and in darkness and measuring the increase in NH,+ and Pod”over a period of 4-6 h. Longer incubation
periods gave equal or slightly lower rates
for NH,+ but significantly
lower Pod”- excretion rates, probably due to adsorbtion
or bacterial assimilation. At stations 2 and
8, the increased NH,+ flux due to macrofauna (bivalves)
in the undisturbed
cores was also measured and compared
with their excretion
rate into bottom
water.
Results
NH,+ production
rate and substrateThe rates of NH,+ production
as measured by 15NH,+ dilution
with a mixing
480
Blackburn
Rate
of
NH;
and Henriksen
production
(d)
(n mol
and
incorporation
cmd3 day’)
0 20
LO 60 80
(i)
11x7
0
20
LO
60
80 la0
8
10
12
14
cm
Belt
W. Kaftegut
Fig. 3. The mean rate of NH4+ incorporation
below sediment surface. Results are for July.
E. Kattega
(i-0)
technique and by an injection procedure
were similar in muddy sediments (Fig.
2). In sandy sediment (Fig. 2, sta. 5), however, the mixing technique
gave much
higher values than in the other sediments. The rate of NH,+ production
was
taken as the mean of the two results, except for sandy sediments (sta. 5, 13). The
injection procedure was not used in November; all November rates are, therefore, from mixed experiments
only and
will not be extensively
discussed. The
mean of the two rate parameters (d and
i) were plotted vs. depth for the four geographically
different
regions (Fig. 3).
Rates in the Belt and western Kattegat
decreased with depth in the sediment. In
the eastern Kattegat there were peaks in
one rate at 4 cm and at 8 cm in the other.
The Skagerrak stations were unique in
having no net ammonium production (d =
i) from 0 to 6 cm and a positive NH,+ uptake (d < i) from 6 to 12 cm. The peaks
in rates below the sediment surface were
probably due to infaunal activity, but the
overall differences
in rates were principally due to differances in the composition of the organic matter in the sediment. The Belt, western,
and eastern
Kattegat stations had positive net NH,+
production and also had the highest mean
N:C ratios; the Skagerrak stations generally had the lowest N:C ratios (Table 1).
and production
t
Skagerrak
(Cl-O)
at all stations
vs. depth
There was a slight decrease in N:C ratio with sediment depth, perhaps indicating some preferential
mineralization
of organic N, but for integrated rates of
NI&+ production
the mean N:C ratio of
the organic matter undergoing
decomposition (Ns) might be expected to be
close to the N:C ratio of the organic matter at the sediment surface. The surface
N:C ratio was selected because the highest rates of d and i were observed close
to the surface, and surface organic material is mixed downward (Blackburn 1980).
Further evidence for downward
mixing
is seen in the almost constant profiles of
organic matter, organic C, and N with
depth (Table 1). Calculations based on the
measured N:C ratios at different depths
are not reliable in the lower strata, where
d and i are low and relatively inaccurate
(Table 1). N:C ratios of cells. and substrate can be related to the ratio d:i as
follows (Blackburn
1980):
E = NslNc
x ild
(where Ns is N:C in the substrate, NC is
N:C in cells, and E is efficiency of carbon
incorporation).
A mixed population of fermenting
and sulfate-reducing
bacteria
might be expected to have NC = 0.16 and
E = 0.3 (Blackburn
19791,). For varying
Ns and d:i ratios, the calculated E values
had a mean of 0.32 & 0.14 (Table 1). As
Sediment
nitrogen
481
cycle
Table 1. Sediment properties
shown were measured in July, except for November temperatures
(in
parentheses).
Mean values are given for organic content and porosity. Integrated values (O-14 cm) are
given for the following:
NH4+ex (exchangeable)
and NH,+pw (porewater)
in mmol NH4+*mm2, for C and
N in mol*m-2, ford (NH,+ production)
and i (NH,+ incorporation)
in mmol.mW2* d-l. Values of E (efficiency
of C incorporation)
were calculated as described in the text; mean values of E were from N:C ratio at O2 cm and integrated d and i values.
Sta.
2
Sediment
section
(cd
Water
depth
(14
O-2
2-4
4-6
6-8
8-10
lo-12
12-14
25
NH,+ex
Temp
(“C)
O-2
2-4
4-6
6-8
8-10
lo-12
12-14
15
(1%)
Mean/integration
5
8
13
14
o-2
2-4
4-6
6-8
8-10
lo-12
12-14
14
Mean/integration
O-2
17
2-4
4-6
6-8
B-10
lo-12
12-14
Mean/integration
O-2
25
2-4
4-6
6-8
8-10
lo-12
12-14
^
Mean/integration
2-4
O-2
4-6
6-8
8-10
10-12
12-14
23
(2)
10.0
(7.6)
(1;::)
Mean/integration
6
O-2
43
(El)
Nf14+pw
(nm019 cm+)
C
N
E
i
d
(nmol.cm-“.d
(jbmol . cmmn)
‘)
iso
8
iii
8
0.36
0.49
0.38
0.39
046
0:54
0.58
17.6
129
145
163
162
166
155
159
7.1
72
52
56
52
36
12
4
5.1
28
18
28
36
36
28
4
0.44
0.25
0.22
0.31
0.43
0.61
1.39
0.60
218.2
268
270
415
281
287
429
429
21.6
34
29
36
24
25
25
25
5.7
108
56
28
28
28
24
24
3.6
90
50
40
0
0
0
0
0.41
0.67
0.60
0.77
2
10
0
0
6.7
40
70
175
190
200
220
230
47.6
1,574
1,526
1,361
1,258
1,147
1,193
1,945
4.0
140
131
117
113
98
102
147
5.9
140
80
32
16
16
16
16
3.6
84
28
24
10
10
12
8
0.49
0.33
0.19
0.40
0.35
0.34
0.40
0.24
0.73
0.65
0.58
0.54
0.53
0.54
0.55
0.56
16.4
230
160
150
230
220
120
120
22.5
15
20
35
45
50
65
65
200.1
1,062
1,125
1,260
1,292
1,314
1,342
1,342
17.0
3.5
12
10
10
16
20
20
20
0.31
z:
46
56
48
48
6.3
40
46
46
48
50
52
52
3.7
2.4
2.1
2.0
2.2
1.8
1.7
1.7
0.56
0.60
0.55
0.54
0.53
0.48
0.45
0.45
24.6
275
230
220
240
280
260
250
5.9
15
25
6.8
50
55
67
79
63
75
86
6.7
128
88
2.2
36
24
zi
15
14
16
174.7
678
743
898
1,040
856
996
876
2.0
7.6
7.4
0.51
0.86
0.81
35.1
140
140
2.6
15
25
121.7
1,010
1,159
9.5
87
87
7.4
108
68
340
350
280
180
120
60
60
35
60
70
110
150
180
180
1,232
1,358
1,399
1,421
1,430
1,371
1,371
121
137
125
127
117
127
127
6.8
14.8
13.2
13.0
13.2
13.0
12.7
12.7
0.79
0.85
0.89
0.90
0.89
0.91
0.90
0.91
27.8
290
275
340
310
300
280
290
15.7
100
180
115
135
150
160
170
191.6
1,254
1,433
1,631
1,614
1,688
1,627
1,664
13.2
0.7
0.8
1.0
0.8
0.6
0.7
0.89
0.42
0.41
0.41
0.40
0.40
0.40
0.40
41.7
760
610
420
290
190
100
100
20.2
60
60
40
50
60
50
50
0.8
9.8
6.5
0.41
0.79
0.73
0.72
0.71
0.71
0.74
0.71
49.4
440
280
6.6
3.8
3.8
3.7
3.6
3.7
3.5
;*i
5:4
5.7
7.5
11.8
Porosity
(ml.cm-S)
0.80
0.80
0.79
0.77
0.79
0.80
0.79
8.0
7.0
6.8
6.4
6.2
6.3
Mean/integration
3
Organic
(% dry wt)
120
68
50
40
t:
28
24
16
70
52
34
28
it
12
6
0
2.5
52
44
0.06
0.06
0.08
0.11
0.09
0.09
0.06
0.13
0.12
0.23
0.29
0.20
0.12
0.15
0.26
0.36
Blackburn
482
Table
1.
Sediment
section
(4
sta
Continued.
Water
depth
(4
NH,+cx
Temp
(“C)
4-6
6-8
S-10
lo-12
12-14
Mean/integration
O-2
65
2-4
4-6
6-8
S-10
10-12
12-14
9
Mean/integration
10
O-2
73
24
4-6
6-8
8-10
LO-12
12-14
11
Mean/integration
O-2
65
4.8
7.0
6.7
4-6
6-8
S-10
l&12
12-14
12
and Henriksen
Mean/integration
O-2
200
24
4-6
6-8
8-10
l&12
12-14
Mean/integration
Organic
(% dry wt)
7.2
7.1
6.6
6.8
0.80
0.78
0.76
0.71
0.71
7.1
12.4
12.2
12.0
11.9
11.8
0.74
0.91
0.88
0.85
0.85
0.86
0.86
0.86
12.1
10.1
9.8
9.8
9.5
9.4
9.3
9.1
0.87
0.84
0.81
0.81
0.81
0.83
0.81
0.81
9.6
7.3
6.7
6.6
6.4
(nmol.
140
110
100
90
90
NH4+pw
cmm8)
C
(pmol.
25
50
70
90
90
1,225
1,214
1,352
1,411
1,411
16.2
80
60
7.3
20
20
;oo
70
;:
30
40
40
175.6
939
1,133
1,206
1,216
1,296
1,296
1,296
9.8
170
470
320
260
260
200
170
3.9
35
75
120
190
250
275
310
0.82
0.69
0.63
0.63
0.64
0.62
0.59
0.56
37.0
350
400
280
240
190
150
120
25.1
35
50
6.4
11.0
10.5
10.0
9.8
9.2
0.62
0.84
0.80
0.73
0.73
0.72
0.70
0.70
34.6
340
240
155
190
320
340
340
10.1
0.75
38.5
Z:l
5.5
6.5
Porosity
(ml.cm-3)
2
this was close to the theoretical value of
0.3 and was relatively
constant, we conclude that variations in d and i values are
related in a meaningful way to significant
variations in sediment N:C ratios (0.039
0.099) and that d and i are themselves
meaningful
rates.
There was considerable variation in the
sediment N:C ratio (Table 1). The reason
for this variation is seen when the N:C
ratio of the upper O-2 cm of sediment is
plotted against the log of the water depth
E
90
95
100
10.2
30
30
z:
65
110
110
8.6
N
d
(nmol*
cn+)
91
99
96
104
104
i
E
cm +. d-‘)
24
14
15
14
13
14
8
8
8
8
0.27
0.29
0.24
0.26
0.30
13.4
60
71
75
79
80
80
80
5.1
50
24
24
20
20
20
20
2.8
24
20
16
14
14
14
14
0.30
0.19
0.33
0.26
0.27
0.27
0.27
0.27
167.6
1,329
1,409
1,415
1,367
1,472
1,562
1,709
10.5
84
85
81
81
81
85
90
3.6
80
152
96
72
48
40
40
2.3
36
48
56
48
40
32
32
0.26
0.18
0.12
0.21
0.25
0.29
0.27
0.27
205.1
1,341
1,534
1,555
1,535
1,578
1,580
1,686
11.7
69
72
70
73
68
64
60
10.6
56
84
94
40
24
18
12
5.8
40
64
80
i::
36
12
0.22
0.23
0.22
0.24
0 66
0’90
0:50
0.22
216.2
1,233
1,600
1,924
2,066
1,934
1,951
1,951
9.5
74
88
106
111
109
102
102
6.6
32
42
8.0
48
60
64
68
70
32
32
0.39
0.56
0.49
0.46
0.44
0.44
0.26
0.26
253.2
13.8
6.2
7.5
0.45
ii
56
40
40
(Fig. 4). The N:C ratio decreased with increasing water depth (omitting
sta. 13).
The regression line cut the axis at 0.16 N:
C, close to the composition
of algal cells
(Redfield 1934). Data for both November
and July are plotted, and in all cases July
N:C was greater than that for November.
There was also a good negative correlation (R = -0.78) when the mean N:C ratio in the lower sediment layers (214 cm)
was plotted against log of the sediment
depth (data not presented). The regres-
Sediment
,000
002
0.04
I
N:C
0.06
I
rot/o
0.08
0
IO-2cml
0.10
,
0.12
I
,I
=
0-U0
0.16
nitrogen
cycle
0.76
A
16
oo= 0.163
m = -0.052
R = -0. El
N
J
N
J
N
J
N
J
NJ
B
Fig. 4. Sediment N:C molar ratios (0-2-cm sediment layer) vs. log of water depth. N:C ratios were
from November (0) and July (0). Station 13 not included in regression lint.
sion line extrapolated to a value of 0.15.
The lower N:C values in November for
the 0-2cm layer were not observed for
the 2-14-cm layer.
NH*+ production
rute und NH4+ poolIncreases in the integrated rate d resulted in increases in total NH,+ pool (Table
l), d = NH4+ pool x 0.068 + 3.61 (R =
0.61). The correlation
between rate and
product (NH,+) gave further confidence
that the rate measurements for the different stations were meaningful.
The rate of
net NH,+ production (d - i), which might
be expected to correlate better with the
NH4+ pool, did not do so.
Another
correlation
between
d and
NH4+ pool is shown in Fig. 5A. The rate
d in the upper O-2 cm of sediment was
higher in July than in November for the
stations sampled at both times (2, 3, 5,
and 8). The increase in d was paralleled
N
J
N
J
N
J
N
J
C
E
?
2
12
r
N
J
6
N
J
0
484
Blackburn
16
1
I
25
-0.6’
-co-
012
Fig. 6. NH,+ flux and NH,+ retained by sediment vs. NH4+ex : NH4+pw. A-Flux
from sediment
to overlying water vs. NH,+ex : NH4+pw in O-2-cm
sediment layer for all stations sampled in July. BRetention by sediment (net production
minus total
and Henriksen
3 by an increase in NH4+ex in Tulv (Fig,
5k3). There was also an increase in ‘Jury
in the ratio of NH4+ex : NH,+pw, as there
was no increase in the NH4+pw (Fig. 5C).
These data indicate that fresh algal cells
were degraded at the sediment surface in
July, giving high rates of NH4+ production. Some of the NH,+ was bound in the
sediment by ion exchange, giving large
NH4+ex pools. In addition to the increase
in NH4+ex, there was an increase in the
efficiency with which NH,+ was retained
in this exchangeable
pool, indicated by
the increased ratio of NH4+ex : NH,+pw.
These three relationships
(Fig. 5) held
only for the upper O-2-cm sediment layer; no similar correlations were found below this, giving further evidence that the
input of fresh organic matter was the
prime agent in producing the effect.
NH4+flux from sediment-The
ion exchange capacity is very important in controlling NH4 + flux from the sediment to
the overlying water (Fig. 6A). There was
a negative correlation (R = -0.89) when
the ratio NII,+ex : NH,+pw (O-2 cm) was
plotted against the flux from sediment to
water for 10 of 11 stations sampled in July
(sta. 5 was omitted because of its high
benthic
algal content).
Where the exchange capacity of the sediment was high,
very little NH4+ was transferred to the
water. As might be expected, there was a
positive
correlation
between exchange
capacity and retention
of NH4+ by the
sediment (Fig. 6B). A plot of the ratio of
NH4+ex : NH,+pw against NH,+ retained
by the sediment gave a positive correlation (R = 0.94) for eight stations (11 and
12 excluded, 5 not plotted). This rate at
which NH,+ was bound in the sediment
was derived from (d - i) minus the flux
of N from the sediment as N03-, NH4+,
and N2 (see Fig. 8). Sediments from a specific geographic
region showed some
similarities
in these plots of flux vs. binding capacity (Fig. 6).
The NH4+ flux in different geographic
N flux from sediment) vs. NH4+ex : NH,+pw in 0-2cm sediment layer for all stations sampled in July.
Regression
line does not include stations 11 and 12.
Sediment
nitrogen
cal regions did not vary significantly
between November and July, except for the
western Kattegat, in which there was a
net uptake in July (Fig. 7). This is also
seen in Fig. 5, where these stations were
distinct from the others. This net uptake
of NH,+ was associated with a high ratio
NH4+ex : NH,+pw (Fig. 5) but was also
due to a high benthic primary productivity, especially at station 5. The NH,+ flux
was not correlated significantly
with organic content of the sediment, d - i, water
depth, temperature, or NH,+pw gradient.
NH,+ oxidution and N export from sediment-The
rate of nitrification
and NO,flux have been reported elsewhere (Henriksen et al. 1980). The flux of NOs-,
sediNJ&+, and PO,“- for the different
ment types for November and July are
summarized in Fig. 7. Neither NH4+ nor
N03flux showed
marked
seasonal
changes, but there was a slightly higher
flux in July than in November. In July,
when there had been a net uptake of NH4+
at the western Kattegat stations, there was
also a relatively small NO,- and POd3- flux
from the sediment, presumably
due to
uptake by benthic algae. In November
37% of the total flux (NO,- + NH,+) was
as NO:,-, compared to 62% in July. In the
Belt and eastern Kattegat there was no
difference in the combined NH4+ + NO,flux between July and November.
The NO,,- flux was not correlated with
any sediment parameter (organic content,
nitrate
gradient,
temperature,
water
depth) other than the rate of nitrification.
That proportion
of N03- production
which did not flux from the sediments is
assumed to have been denitrified,
probably a correct assumption for most stations, but some N03- may have been assimilated by benthic algae, particularly
at
station 5 in July. The Pod”- flux is discussed later in relation to denitrification.
All the measurements presented were
made in undisturbed
sediment cores in
Plexiglas tubes that contained no visible
macrofauna. These fluxes and the various
rates of NH,+ and N03- production
for
station 8 in November and July are shown
in Fig. 8 as an example of how N cycled
in a specific sediment.
485
cycle
JULY
NOVEMBER
1.0,
-im
';J
E
z
E
06
0.L
0.2
0
W
Fig. 7. NIL+ (solid), NO,- (shaded), and P04”(open) flux from sediments. July: B-stations
2 and
3; W-stations
5,8, 13, and 14; E-stations
6,9, and
10; N-stations
11 and 12. November:
B-stations
2 and 3; W-stations
5,8, and 14; E-station
6 (Henriksen et al. 1981).
Although d and i were higher in July
(1OOC) than in November (7.6”C) the net
rates of production
(d - i) were almost
identical. In July there was no NH,+ flux
to the water, whereas in November 39%
left the sediment. In July, 67% of the d i entered an exchangeable
pool, compared with 26% in November.
In both
November and July there were equal rates
of nitrification
(34% of d - i). In November NO,- flux from the sediment
was
larger and denitrification
was smaller than
in July.
Effect of benthic fuuna-To
determine
the effect of the benthic infauna on the
flux of inorganic N and P from the sediment, we measured the excretion rates of
NH,+ and PO,“- by the quantitatively
most important groups of infauna at each
station (Fig. 9). There was some variation
between stations, as would be expected,
-
A
486
Blackburn
and Henriksen
NOVEMBER
Bound
JULY
Bound
Fig. 8. Model of N cycling in sediment.
ammonium is that portion of net production
flux to overlying water.
N2
Oata are from station 8. All rates in mmo1*m-2*d-‘.
Bound
which is bound by ion exchange and does not immediately
due to differences in species composition,
size, food sources, and temperature. There
was, however, good agreement between
measurements in November and July for
the different groups.
The effect of benthic infauna on the rate
of nitrification
was not systematically
examined, except at station 5 where we incubated intact worm burrows, still containing
individuals
of the dominant
species (La&e
conchilegn)
in seawater
under oxic conditions
at in situ temperature and NH,+ concentration.
Nitrification rates in the tube walls, measured as
NO,- + N03- accumulation,
were 1,600
nmol NH,+ oxidized *cm-“. d-l in November and 2,900 in July. The nitrification
rates measured in the tube walls can be
considered
near in situ conditions
and
would increase the nitrification
rate per
sediment surface area by 0.22 and 0.14
mmol NH4+ oxidized *rne2. d- ’ for November and July (200 ind *rnh2 in November and 140 in July).
Discussion
The results can be conveniently
discussed with reference to Fig. 8, in which
the main parameters measured can be
seen in relation to each other.
Some evidence for the validity of the
rates d and i is seen in the increasing
ratios of i : d corresponding
to decreasing
ratios of N:C in the fresh substrate, yielding a constant C assimilation
efficiency.
There is, however, a mean decrease of
10% in N:C ratios with sediment depth
(Table 1). This means that substrate of a
higher N:C ratio than that measured in
the O-2-cm stratum was degraded. Nitrox sedigen accumulation
(concentration
mentation
rate) may be expressed as a
proportion of N input (accumulation
+ N
efflux: see Tuble 3), which is used to calculate the N:C ratio of the actual substrate degraded. For stations 6, 9, and 10,
the sedimentation
rates were 0.05, 0.16,
and 0.62 cm. yr-’ (Jargensen pers. comm.),
proportional
accumulations
of N were
Sediment
nitrogen
Nl
$;i::::
.::::::
:.
::::::
.:.x.
$$>.;
:.s
487
cycle
0
4
(shaded) and July (open).
Fig. 9. Specific excretion rates of NH,+ and POd3- in November
noidea (Echinodernta
and Brissopsis);
%Ophiuroidea
(O$k.wu
and Amphiuru);
3-Polychaeta;
mellibranchia.
0,07,0,16, and 0.49, and N:C ratios in the
actual substrate were 0.087, 0.064, and
0.070 (1, 0, and 5% above those measured), These differences would not seriously change the calculated values of E.
We thus predict that net uptake of NHiC
will occur when Ns < 0.05 (E = 0.3, NC =
0.16 d = i). Net NH,+ uptake was observed
only at stations 11 and 12, which had the
lowest N:C ratios (0.044 and 0.055), except for station I3 which was anomalous
in other respects (see Fig. 3 und Table 1).
Variations in sediment N:C ratio corresponded
with variations
in rate processes and were also related to the log of
water depth. The value for the N:C ratio
at O-2 cm for July and November (n = 16)
fitted the regression N:C = 0.163 - 0.052
log r-n depth (R = -0.81). The extrapolation to 0.163 at the water surface fits very
well with the interpretation
that algal cells
produced in the photic zone sank through
the water column and were progressively
mineralized.
Models have been proposed
to describe carbon mineralization
as a
function
of water depth (Suess 1980;
Suess and Miiller
1980). Nitrogen mineralization
has not been similarly
modeled but there is preferential
degradation
1-Echi“La-
of nitrogen in sedimenting detritus (Suess
1980; Suess and Miiller
1980; Honjo
1980). Our data, which are from lo- to
200-m water depth, cannot readily be
compared
with the C mineralization
models, which are primarily for deep-sea
sediments.
Our model
can predict
changes in the relative quantities of N and
C but gives no information
on the actual
amount of each that is mineralized.
It is
doubtful that the relationship
would hold
for depths >lOO-200 m, since there must
be a lower limit below which the N:C
ratio cannot fall.
The nitrogen input to the sediment can
come from three sources: the phytoplankton, the benthic algae, and unknown terrestrial material. The ratio of total N flux :
phytoplankton
N productivity
represents
the extent to which phytoplankton
debris
could have contributed
nitrogen to the
sediment. In the Belt Sea, western Kattegat, and eastern Kattegat, 36-61%, 3892%, and 58% of the phytoplankton
N may
reach the sediment surface. These values
are in the same range as 45% for Narragansett Bay (Nixon et al. 1976) and 3662% for the southern bight of the North
Sea (Billen 1978). Presumably
much of
488
Blackburn
and Henriksen
the phytoplankton
sedimented during the
spring- bloom, before zooplankton
grazing became significant
(Smetacek 1980).
Our values are compatible with a deposition of 30-40% of the primary productivity to a variety of sediments from the
water column (Parsons et al. 1977).
The contribution
of benthic algae to N
mineralization
in these sediments may be
high for stations with ~20 m of overlying
water, particularly
for the sandy stations
in the western Kattegat. Steemann Nielsen (1973) estimated that benthic productivity could be 45% of planktonic productivity. At station 5 the benthic productivity
was ~70 mg C *rne2. d-” in July: 30-100%
of the phytoplanktonic
production
(N. P.
Revsbech pers. comm.). The contribution
from terrestrial sources is unknown
but
was probably quite small except in parts
of the eastern Kattegat where rates of accumulation were high (Rohde 1973; Genders and Larsen 1976).
An interesting aspect of the N: C to depth
relationship
(Fig. 4) was the seasonal
variation in N:C (O-2 cm) and the effect
of depth on the magnitude of this variation. In all cases, the July N:C was
greater than the November ratio; the difference became less with increasing water depth. The data suggest that fresh
algal cells produced in the photic zone
before July had fallen to the sediment
surface; the shallower the water, the less
N was mineralized
in the water column.
Between July and November, most of this
readily degradable N had been mineralized at the sediment surface.
The model (Fig. 8) shows how the rates
of ammonium
production
and uptake
were influenced by the change in N:C at
the sediment surface, July being much
more active than November due to the
higher sediment N:C (&2 cm) (Fig. 4).
In addition to the correlation between
rate (d and i) and substrate (N:C), there
is also a relationship
between rate and
product ( NH4+ pool) :
d = 3.61 + 0.068 x total NH,+ pool
(I? = 0.61).
The rate d may thus be calculated from a
simple pool measurement.
A further re-
lationship
between d and pool was observed. In the 0-2-cm sediment stratum,
the value of d (Fig. 5A) and NHq+ex :
NH4+pw (Fig. SC) was always higher in
July than November.
Rosenfeld
(1979)
showed that NH,+ exchange activity was
associated with organic material in sediment. It is possible that degradation
of
organic material created transitory
sites
for NH,+ exchange. These sites, possibly
carboxyl groups, would themselves have
been largely degraded by November.
The exchange
capacity
(NH4+ex :
NH,+pw) was a very important parameter
in determining
the fate of the surplus ammonium (d - i) in the sediment. A high
exchange capacity was inversely related
to the rate of NH,+ flux from the sediment
and linearly related to the rate of NH,+
transfer to NH4+ex. In these sediments the
exchange capacity appeared to be the
most important parameter in regulating
the supply of NH*+ to the overlying water
and for nitrification.
The model (Fig. 8)
illustrates the high rate of NH,+ transfer
to NH,+ex in July and the greatly reduced transfer rate in November.
Presumably NH;+ accumulated
in this pool
during periods when fresh detritus was
degraded (late spring and summer) and
later entered the NH4+pw during winter
and early spring. The net effect of this
bound pool was to buffer NH,+ flux and
oxidation on a seasonal basis. Thus, the
mean flux of NH4+ from the sediment was
almost the same in November as in July
(Fig. 7), and at individual
stations it could
be higher in November (Fig. 8). The NO,flux was, however, higher in July. Unlike
the many correlations that could be made
between NH,+ pools, d, and rates of entry
to NH4+ex, the NO,- flux could only be
related to rate of nitrification
(Fig. 10).
The correlation
coefficient
was 0.88 for
July and 0.93 for November values. There
was no correlation between organic content of the sediment and rate of nitrification, This is in accord with Billen’s
(1978) observation
that nitrification
was
independent
of organic content of the
sediment when this was >2.0%. Only station 5 had a lower organic content. Nitrate was never taken up by the sediment.
Sediment
nitrogen
About 50% of the NO,- production fluxed
from the sediments in July, compared to
80% in November. There was little seasonal change in total NH4+ + NOs- flux,
but there was a higher proportion of NO,in the July flux (62%) than in the November (37%).
The rate of nitrification
was increased
by the presence of L. conchilega burrows
in the sediment at station 5. The increase
was quite significant,
0.14-0.22
mmol
NH4+ oxidized *rnB2 * d-l, compared with
the normal nitrification
rate, 0.3-1.7, in
the absence of animals
and burrows
(Henriksen
et al. 1981). Even greater increases in the rate of nitrification
(0.5-1.0
mmol *rnm2*d-l) may be attributed to the
higher densities
of Nereis virens and
Corophium
volutator,
which are common in inshore sediments (Henriksen
et
al. 1980). Since rates of denitrification
were calculated from the rate of nitrification minus NO,- flux, changes in denitrification
rate could not be measured.
General denitrification
was indicated by
low N:P flux ratios, and denitrification
mediated by infauna was suggested by a
high denitrification
potential in the burrow walls (J. Sprrensen pers. comm.). A
low N:P flux ratio (5.0-6.5) in the Kattegat
and Belt Sea (compared to 16:l ratio in
algae: Redfield 1934) was similar to that
found by Nixon et al. (1976) for Narragansett Bay, in which extensive denitrification occurred (Seitzinger et al. 1980).
A N:P flux from the sediment
>16: 1
would be expected since the organic detritus that reached the sediment was depleted in N compared to C and was presumably depleted in P compared to N
(Suess and Miiller
1980). Denitrification
seems to be a reasonable explanation
of
low N:P flux ratios.
The N and P fluxes from the sediment
were influenced
by the activity of the
benthic infauna. The infauna had a considerable effect in increasing the NH,+
flux by direct excretion from the animals
and by stimulation
of microbial nitrogen
transformations
in the microenvironment
around the burrows. We have measured
only the excretion rate, but there is evidence that excretion is a good index of
489
cycle
NOV
JULY
1.0 i-
nitrification
-0.2
-
mmol
rate
rnm2d -’
Fig. 10. NO,- flux from the sediment plotted as
a function of nitrification
rate (Hcnriksen et al. 1981).
the contribution
by the infauna to the
NH4+ flux from the sediment. Henriksen
et al. (1982) made the following
observations for sediments similar to those that
we have studied. There was the same relative stimulation
of NH,+ production and
oxidation in the burrow environments
of
infauna of different types (Polychaeta, Bivalvia, and Crustaceae). As a result of this
increased nitrification,
the infaunal NH,+
flux from the sediment
did not differ
greatly from the measured excretion rate
into water (most values were between 80
and 150% of the excretion rate). Similarly, the NH4+ flux due to the bivalves Mucoma calcarecr. and Syndosmya nitidn in
undisturbed
sediment (sta. 2 and 8) was
130-160% of the excretion rate into bottom water.
Increased NH,+ flux due to benthic infauna activity
has been observed frequently
(Aller
1978, 1980; Aller and
Yingst 1978; McCaffrey et al. 1980). It has
been attributed to an increased transport
velocity of ions over the sediment-water
interface (biopumping)
and a stimulation
of microbial NH,+ production in the sediment. Ammonium
excretion by the infauna was considered
of minor importance, but not directly
measured.
In
Narragansett Bay (McCaffrey et al. 1980),
the in situ NH,+ flux from a biologically
disturbed sediment (2.7 mmol NH4+.m-2*
d-l) was compared with the diffusive flux,
490
Blackburn
and Henriksen
calculated from concentration
gradients
(1.9 mmol NH4+ *rnA2. d-l). The contribution from biogenic
infaunal
activity
would here be 30% of the in situ NH,+
flux, in good agreement with our values.
The infauna did not significantly
increase N03- flux. Henriksen et al. (1982)
observed that infauna of different groups
could increase or decrease the N03- flux
from sediments, depending on irrigation
activity, burrow construction,
and NO,concentration
in the overlying water. In
a mixed community
the overall effect of
the infauna on NO,- flux was insignificant.
We used the measured NH,+ excretion
rates (Fig. 9) to quantify the contribution
of the different infaunal communities
to
the NH4+ flux from the sediment. The stations were grouped by use of character
species into five of the eight benthic infaunal communities
described by Petersen (1918). The grouping was a little different from the geographical
grouping
used in Table 1. The species composition
and biomass data of Petersen (1918),
which are still representative
for the area
(IL Okkelmann pers. comm.), were used
together with the specific excretion rates
to calculate the increased NH,+ flux from
the sediment due to the infauna (Table
2). This varied from 0.22 to 0.65 mmol
NH,+ *rne2. d-l, values quite large when
compared to the NH4+ flux from the sediments (0.4-1.0 mmol NH,+. rne2* d-l) in
the absence of infauna. The flux corrected for infaunal contribution
is included
in Table 3.
Phosphate was also excreted by the infauna into the water; there was, however,
no correlation
between these excretion
rates and POd3- fluxes from the sediment.
This is probably
due to adsorption
of
Pods- to the oxidized burrow walls. We
have not attempted to make quantitative
estimates of phosphate fluxes.
Contribution
of sediment nitrogen to
planktonic
primary
production--Because there was little difference between
November and July rates of d - i, the annual budget is based on 12x the July
rates, which were measured for more sta-
Sediment
Table 3. Net mineralization,
or yearly rate-n-m.
nitrogen
N flux, and net productivity
relationships
N
Reference*
1
1
1
2
3
4
4
5
5
5
6
Area
Belt Sea
W Kattegat
E Kattegat
Limfjord
Narragansett Bay
S bight, North Sea
S bight, North Sea
FOAM
NWC
DEEP
Cape Lookout
Depth
hid
lo-30
lo-30
30-100
4-12
7
15
35
10
20
30
10
Net NH4 t
prod.
13.3
18.4
14.3
10.2
n.m.
27.0
12.5
mm.
n.m.
n-m.
n.m.
491
cycle
NII,(’
NO:,
3.6
4.6
7.0
9.1
12.2
9.4
4.6
5.1
7.7
2.4
51.3
2.6
1.7
1.8
4.9
1.5
11.5
6.0
n.m.
n.m.
mm.
n.m.
(g N*mP. yr-l). No measurement
flux
(NHab
W
Net primary
N prod.
N prod.
1.3
1.8
0.7
4.9
2.6
6.1
1.9
n.m.
n.m.
n.m.
n.m.
7.5
8.1
9.5
18.9
16.3
27.0
12.5
-
12.3-21.1
8.8-21.1
16.5
17.1-35.2
38.7
19.3-33.4
20.2-35.2
24.5-29.3
24529.3
24529.3
mm.
0.29-0.50
0.30-0.72
0.53
0.40-0.82
0.35
0.63-1.08
0.30-0.52
-
* l-This
investigation.
Net NII, I- production
calculated
from 12x July values. N fluxes calculated
as means of November
except for western Kattegat (3x July rate, 9x November
rate) where benthic algal activity was limited to high light intensities
Increase
in NIIdk flux due to benthic
infauna
is included.
Net primary
N production
rates calculated
from gross primary
(Steemann
Nielsen et al. 1978), correct4
to net primary
production
(75% of gross production:
Jcnasson 1972), and coverted
N production
by use of Redficld ratio (N:C 1:0.15) in algal cells. 2-Blacktnun
and IIcnriksen
(unpubl.
data). 3-Nixon
et al.
et al. 1960. Values for NO,- flux and Nz flux are summer values, calculated
for a 6-manth
pcriad. 4-Billen
1978. 5-Aller
and Martens
1981. This was calculated
by integrating
figure values for seasonal changes in NH, c flux.
tions (Table 3). These rates (13.3-18.4 g
N *me2 *yr-‘) are a little higher than in the
Limfjord (10.2) but lie within the range
(12.5-27.0) quoted by Billen (1978) for the
southern bight of the North Sea. The fluxes of nitrogen (NH4+, Non-, N2) from the
sediment were 56,44, and 66% of the rate
d - i for the areas of the Belt Sea. western Kattegat, and eastern. In the Limfjord
d - i was apparently less than the total N
flux (18.9 g N*m-2.yr-1).
The large difference between net NH4+ production and
net N flux from the sediment of the western Kattegat probably reflects the benthic
algal assimilation
of NH,+ at the sediment surface. The algal cells may then
h ave been mineralized
in the sediment.
This benthic algal production
may also
explain why gradients of NH,+ in the sediment pore&ater were not correlated with
NH,+ flux from the sediment of the western Kattegat.
In the eastern Kattegat and the Belt Sea,
there was no significant seasonal trend in
the inorganic nitrogen (NO,- + Nod+) flux
from the sediment (0.9-1.3 mmol N*rne2*
d-l). Only in the western Kattegat, was
there a seasonal variation, with low inorganic N flux in July (0.18 mmol N *m-2.
d-l) due to high ratios of NH4+ex :NH,+pw
in the surface layer and to the presence
+ NO,-)
t:
and July values,
in midsummer.
C production
to net primary
1976; Seitzinger
1980. 6-Klump
of benthic diatoms. The apparent lack of
seasonal variation in most parts of the area
investigated
agrees with results from the
southern bight of the North Sea (Billen
1978) and may be due to several factors.
The difference
between maximum and
minimum
temperatures
at the sediment
surface was small (7.5”-10.3”C) with maximum temperatures of 12”-14°C (Nielsen
1976). Large amounts of easily degradable algal detritus may fall to the sediment
surface after the phytoplankton
spring
bloom when grazing by the zooplankton
in the water is delayed and temperatures
at the sediment surface are still low. Furthermore,
the buffering
effect of the
{higher exchange capacity for NH4+ at the
sediment surface will tend to smooth out
the NH4+ release from the sediment. The
low seasonal variation and the relatively
low variance between stations within the
sampling area has allowed us to calculate
an approximate annual budget for the efflux of inorganic nitrogen from the sediments, using the mean values for November and July (Table 3). The Skagerrak
sediments were sampled only in July and
these data are not included. The-estimated rates of NHA+ release due to the benthic infauna were added to the diffusional flux, using the values for the dominant
492
Blackburn
and Henriksen
infaunal communities
found in the dif’ferent parts of the area (Table 2). The annual release of NH,+ + NO,- ranged fi-om
6.2 to 7.8 g Nmrne2. yr-‘. The estimated
contribution
due to the benthic infauna
ranged from 30 to 60% of the NH4+ flux
to the water. These values indicate the
importance of benthic infauna in the regeneration of inorganic nutrients from the
sea bottom. In the southern bight of the
North Sea the contribution
of macrofauna
to benthic recycling of N was estimated
to be 20% of the bacterial contribution
(Billen 1978). Denitrification
was equivalent to 21-31% of the NH,+ + NOnm flux
from the sediment. It is probable that the
activity of the benthic infauna would increase the rate of denitrification,
but
quantitative
estimates of this effect could
not be made. We consider the reduction
of NO,- to NH,+ to be insignificant.
More NH,+ than NO,- was released
from the sediment of the Belt Sea and
western and eastern Kattegat. This was
also true for the shallow water sediments
of the Limfjord
and Narragansett
Bay,
which had relatively
high summer temperatures.
The release of a relatively
higher proportion
of NO,- is common in
the sediments of deeper waters like those
of the North Sea, which have less seasonal variation in temperature and are possibly more oxidized.
The efflux of NH4+ and NO,- from the
sediments of the Belt Sea and western
and eastern Kdttegat indicated that 3072% of the N requirement
of the primary
producers could be supplied by the sediment. This agrees with the 40-82% contribution
to the planktonic
primary producers in the Limfjord and the 30-108%
.for the North Sea. The data quoted for the
FOAM, NWC, DEEP, and Cape Lookout
sites in Table 3 are less complete and do
not permit this type of estimation.
It
would seem likely from the NH4+ fluxes
at FOAM, NWC, and DEEP, which are
similar to our values, that those sediments also contribute
significantly
to
planktonic
N nutrition.
The very high
NH4+ flux from Cape Lookout sediments
(51.3 g N*m-2*yr-1)
must make a very
large local contribution
the phytoplankton.
to the nutrition
of
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Submitted: 30 July 1981
Accepted: 19 October 1982