Pathways of organic carbon oxidation in three continental margin sediments

Marine Geology, 113 (1993) 27-40 Elsevier Science Publishers B.V., Amsterdam

27

Pathways of organic carbon oxidation in three continental margin sediments D . E . C a n f i e l d a, B.B. J o r g e n s e n b, H . F o s s i n g b, R. G l u d b, J. G u n d e r s e n b, N . B . R a m s i n g b, B. T h a m d r u p b, J . W . H a n s e n c, L.P. Nielsen c a n d P.O.J. H a l l d

aEarth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA 30332-0340, USA bMax Planck Institute for Marine Microbial Ecology, 2800 Bremen 33, Germany Clnstitute of Biological Sciences, ,,frhus Univ., Bid. 540, D K 8000, .~rhus C, Denmark dDepartment of Analytical and Marine Chemistry, Univ. of G~tenborg, S-412 Gi3tenborg, Sweden (Revision accepted April 27, 1993)

ABSTRACT Canfield, D.E., Jorgensen, B.B., Fossing, H., Glud, R., Gundersen, J., Ramsing, N.B., Thamdrup, B., Hansen, J.W., Nielsen, L.P. and Hall, P.O.J., 1993. Pathways of organic carbon oxidation in three continental margin sediments. In: R.J. Parkes, P. Westbroek and J.W. de Leeuw (Editors), Marine Sediments, Burial, Pore Water Chemistry, Microbiologyand Diagenesis. Mar. Geol., 113: 27-40. We have combined several different methodologiesto quantify rates of organic carbon mineralization by the various electron acceptors in sediments from the coast of Denmark and Norway. Rates of NH~ and I~CO2liberation in sediment incubations were used with 02 penetration depths to conclude that 02 respiration accounted for only between 3.6-17.4% of the total organic carbon oxidation. Dentrification was limited to a narrow zone just below the depth of 02 penetration, and was not a major carbon oxidation pathway. The processes of Fe reduction, Mn reduction and sulfate reduction dominated organic carbon mineralization, but their relative significance varied depending on the sediment. Where high concentrations of Mnoxide were found (3-4 wt% Mn), only Mn reduction occurred. With lower Mn oxide concentrations more typical of coastal sediments, Fe reduction and sulfate reduction were most important and of a similar magnitude. Overall, most of the measured 02 flux into the sediment was used to oxidized reduced inorganic species and not organic carbon. We suspect that the importance of 02 respiration in many coastal sediments has been overestimated, whereas metal oxide reduction (both Fe and Mn reduction) has probably been well underestimated.

Introduction A diverse population of microorganisms, utilizing a variety of electron acceptors, is responsible for the oxidation of organic matter in marine sediments, and a large literature has explored the rates and relative importance of the different carbon oxidation pathways (e.g. J~rgensen, 1977, 1983; Reeburgh, 1983; Bender and Heggie, 1984; Henricks and Reeburgh, 1987; Reimers et al., 1992; Canfield, 1989, 1993). Our ability, however, to fully understand the processes o f carbon oxidation has been confounded by our inability to measure directly the rates of m a n y of the oxidation pathways. F o r example, there is not yet a direct assay 0025-3227/93/$06.00

for heterotrophic 0 2 respiration, the rates of which have been inferred from rates of sediment 02 uptake, after accounting for the 02 used in oxidizing reduced species other than carbon (e.g. H2S, Fe 2 +, M n 2 +, and N H ~ ) . An accurate determination of O 2 respiration, then, requires an accurate knowledge of the production rates of reduced species. There is also no direct assay for Fe oxide and Mn oxide reduction, hence, carbon oxidation rates and reduced species production by these processes are uncertain. Direct assays are available for denitrification (Sorensen, 1978; Nielsen et al., 1992), sulfate reduction (Jorgensen, 1978; Fossing and Jorgensen, 1990), and methanogenesis (Crill and Martens, 1986; Kuivila et al., 1990), and their

© 1993 - - Elsevier Science Publishers B.V. All fights reserved.

28

D.E. C A N F I E L D

importance in carbon oxidation is relatively well known (Jorgensen, 1982; Reeburgh, 1983; Canfield, 1993). In what follows we evaluate the significance of all of the major processes of carbon oxidation in 3 different sediments from coastal Denmark and Norway. We apply a variety of analytical techniques to determine rates, including direct assays for sulfate reduction and denitrification, rates of sediment 02 uptake, 02 depth distributions, and discrete interval sediment incubations. Although we still have not measured directly rates of 02 respiration and metal oxide reduction, we are able to constrain their rates by accounting for the rates of the known processes. With these estimates we reevaluate the importance of 02 respiration and metal oxide reduction in coastal sediments.

Study sites Three sites in the eastern Skagerrak were sampled between September 2 and September 14, 1991 (Fig. 1). The clay content of the sediment increased from the basin margin to the interior (Fig. 2), and the sites ranged in water depth from 190 meters at S#, to 380 m at $6, and 695 m at $9. Sediment deposition rates at these sites have not been measured, but Van Weering et al. (1987) reported rates of between 0.1 to 0.2 cm yr- ~ in the area. Substantial infaunal burrow networks were revealed at all sites by visual inspection and X-radiographs on intact cores. At Sa and $6, we recognized a macrofaunal assemblage of brittle

NORWAY1 , f l ' ; " ,--~ ,, \ ', ,~.~~e,. rt',, ~

j

~lll~r,.'7~."-.-"

,

-

*

~I.

/I /

I

-

\ ~

'?l[¢

~ ;.,~-.

. ~---t. .:,,, ".-.~ ,~ ~J " . . " ;,,: ~,l,~, ~

~'L".~.;.~-:-'.~.~'~ . - " .

:_.- _,,e,~~ S~" ~

t,~';"L~

.'

."

;.,.--

,-,,,,-u~.,,

b ~'~/a~

D~NMARKj~~,~I"~ " " ~

Fig. 1. Map of the sampling sites. Only S,, $6 and S 9 are included in the present study.

E T A L.

Sand

I

I si. Cloy

,o o

%Curnulative

80

Total

60 40 20

S2

S4

S6

S7

S8

S9

Station

Fig. 2. Distribution of sand, silt and clay in a transect from $1 to $9. For details on analytical procedure see Canfield et al. (in press).

stars, heart urchins and polycheates, while at $9, the macrofauna was dominated by capitellid polychaetes. One of the major differences between the sites was the very high surface solid-phase Mn content of 3.5-4 wt% at $9. An important part of our sampling strategy was to explore the effects of enhanced Mn oxide availability on the pathways of carbon oxidation.

Methods As this manuscript summarizes and synthesizes results that have or will be published elsewhere, only a brief description of methods will be offered here. Sediment was collected in 10 cm diameter Plexiglas tubes that were fixed to a multicorer frame and lowered very slowly into the sediment (Barnett et al., 1984). This allowed the collection of very undisturbed cores. Rates of 02 uptake were determined on intact cores thermostated to bottom water temperature and stirred with a Teflon coated magnetic stir bar, suspended approximately 2 cm above the sediment surface. The turbulence generated in this system approximates that found at the sediment-water interface in coastal sediments (Rasmussen and Jorgensen, 1992). Rubber stoppers, penetrated by a liquid paraffin-filled hole, were used to seal the water overlying the sediment from gas exchange. 02 microelectrodes with minimal stirring response (< 1%) were inserted through the hole, and the decrease of 02 with time was measured on 4-5 replicate cores. Before making rate measurements, the depth distribution of 02 was determined in a number of places in the

ORGANIC CARBON OXIDATIONIN CONTINENTALMARGIN SEDIMENTS

sediment with 0 2 microelectrodes. The depth distribution of 02 was also measured in situ with a free-vehicle lander (Gundersen and Jorgensen, 1990). Sediment from the multicorer was also sectioned into discrete intervals and incubated at near in situ temperature in gas-tight plastic bags (Hansen, 1992; Kruse, in press). The production rates of NH + (at all sites), ZCO2 (at $6), and Fe 2+ and Mn 2+ were monitored with time. In a separate series of incubations molybdate was added to the sediment to inhibit sulfate reduction and the production of sulfide. Rates of Fe 2÷ and Mn 2÷ liberation from these experiments, when compared to rates in the unamended incubations, indicate whether any Fe oxide or Mn oxide reduction is coupled to the reaction between the oxides and dissolved sulfide. Ferrozine was also added to some of the incubations to bind Fe 2 + and inhibit the potential reaction between Fe 2 ÷ and Mn oxides, as may occur in marine and freshwater sediments (Lovely and Phillips, 1988; Myers and Nealson, 1988). Rates of sulfate reduction were measured with 3~SO2- on splits of the same sediment used for the incubations. Also, sediment collected from the start of the incubations was subjected to a variety of chemical extractions to determine the distribution of acid volatile sulfide (AVS), pyrite sulfur, Fe 3+ in iron oxides, Fe 2+ as extractable nonpyrite phases, Mn oxides, and the oxidation level of extractable Mn at $9. A complete 'accounting of methods used in the incubations, solid phase analysis, pore water analysis, and sulfate reduction rate measurements can be found in Canfield et al. (in press). Denitrification rates were determined using the isotope pairing technique of Nielsen (1992), where 15NO 3 was added to the water of an incubation vessel in which freshly collected, intact sediment cores were inserted and thermostated to bottom water temperature. The cores, with overlying water, were sealed with stoppers after a 10-40 hour preincubation period allowing steady-state gradients of lSNO 3 to be established. Accumulated labelled N2 in pore water and overlying water was extracted after incubation periods

29

ranging from 0 to 50 hours. Rates of denitrification of natural NO3 (14NO~) were calculated from the temporal increase of single labelled versus double labelled N2. Full description of the analytical procedure is given in Nielsen (1992). Results

Rates of sediment 02 uptake and denitrification are given in Table 1. The depth distributions of pore water Fe 2÷, Mn 2+, NO33 , and NH~- are shown in Fig. 3, while the depth distributions of solid phase Mn, Fe and S are presented in Fig. 4. An example of the in situ distributions of 02 at $4 and $9 are shown in Fig. 5. From between four to six profiles were measured at each site, with little variability between profiles. 0 2 profiles measured on sediment returned to the lab were similar to those measured in situ, as were the depths of 02 penetration. No in situ profiles were obtained at $6, but the depth of 02 penetration in lab profiles was about 1.1 cm. Rates of NH~- liberation from the sediment incubations are shown in Fig. 6, and rates of sulfate reduction measured on the same sediment are presented in Fig. 7. Rates of ~CO2 liberation were measured at $6, and these results are given in Table 2, along with NH~ production rates and the ECO2/NH ~ liberated to solution. Fe 2 + and Mn 2 + liberation results are fully discussed in Canfield et al. (in press), but briefly, beginning with $4, Mn 2 ~- was liberated to solution between 0 and 1.0 cm depth, whereas Fe 2 + liberation was observed between 0.5 and 3cm. Comparing liberation rates in molybdate-amended TABLE 1 02 uptake, denitrification, and total carbon oxidation rate Site

02 uptake*

Denitrification b

Total C oxidation c

$4 S6 $9

16.06 (1.17) a 10.38 (2.09) 11.83 (4.5)

0.4 0.3 0.5

15.76 10.15 I 1.23

"mmoles 02 m -2 d -1. bmmoles N m -2 d -1. Cmmoles C m -2 d - I . d( ) = one standard deviation.

30

D.E. C A N F I E L D ET AL.

$4 0

Mn, Fe (pM)

oI

100

5O

150

i

i

200

0

~u' o'8 '

5

10

50

100

0

.2

O

0

o

0..

0 .4

o

0

o -6"

NH4 (p.M)

0

O

-4"

200

150

O0 o

O

-2"

NO3 (p.M)

0

o

.6

•

=-1

o

.8

-8"

-10

Ss Mn, Fe (~M)

0!

25i

.

50 ,

.

75 ,

.

NH4, NO3 (pM) 100

oI

:o •

-4" t,(1) a

.2i

0

-2"

0

50

2=

75

,

i

,

100 J

125

,

i

,0 0 0

-4

0

•

0

0

-6"

25

•

0

0

_6 q

•

-8"

-8"

-10

-10

$9 Mn, Fe (p.M) 200

0

NH4, NO3 (pM)

400

600

0

20

o ,,c~ ,, ~ 0

40

. . . . .

60

80

O

0 0 •.4-2

~E

-4,

~

-6'

0o

0

o 0

-6 o -10

0

l 0

-10'

Fig. 3. Pore water chemistry at $4, S6, and $9. A single multicore was processed for each site.

and unamended incubations, there was no evidence for the sulfide-mediated liberation o f Fe 2+ or Mn 2 + to solution. As discussed by Canfield et al. (in press) the observed liberation o f Mn 2 + between 0 and 0.5 cm may have been an experimental

artifact arising from the early consumption of 0 2 and NO~- in the incubations. It is not clear that Mn 2+ liberation would occur naturally in this interval with 0 2 and N O a present. At $6, Mn 2 + liberation was observed between 1

ORGANIC CARBON OXIDATION IN CONTINENTALMARGIN SEDIMENTS Mn, ~ m o l e s c m "3

Mn, l~moles c m - 3 0 1 2 0 . . . . . .

31

3 @'

1 2 . . . . .

Ol

Mn, ~moJes cm-3

3

0

'@'

50

100

150 200 @' " • •

0 '0 . . . . . 0 0

-2~

-2.

-2'

0

•

0 -4.

-4

-4"

-6 ¸

-6

-6"

-8

-8'

-8"

•

J=

@0

•

S4

•

$6

-IO

-1o

S, i l m o l e s

o'

S, ~trnoles c m - 3

cm-3

5 10 '0 . . . . 0

"

-10

15

20 0

3 I

,

6 i 0 ,

,

9 I

12 0

0

•

"2

0 •

0 0 0

.4

•

0

0

6

-6.

0

•

-8"

0 •

S6

0

20 i •

O'& 0 0

-2"

6o @l

• 0

0

0

•

•

i

S9

20 '

40 ' 0'

"

CL 0 • .2

•

0

-10

0 ° J fl,~

• •

0

Fe t~moles c m - 3

40

Fe p m o l e s 60 i •

2

50 , i

cm-3

1O0 '

150

'0'

'

200 "

•

0

•

0

-4"

• •

•

-4

0

•

0

-6"

;L

@A

•

-6.

'

0

•

•

0

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L

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•

-8-

-8" S4 -10

•

0

0

, -8-

Fe ~ m o l e s c m - 3

~ D

0

8

-lO

0

-4.

0

$4

2 3 . . . .

-2

0

0

-4. •

1 ' 6 0

'

0

0 -2.

S, ~ m o l e s c m "3

Oe

•

0

•

•

$6

'A

•

S9

-10,

@ Fe fill) J ~ Fe(ll) Fe S-bound

I

Fig. 4. Solid phase Mn, sulfur and Fe at the different sampling sites. For M n at $9, only oxidation levels of 4 + and 2 + were assumed. All measurements were made on sediment used for the incubations, but collected before the incubations were begun.

and 2 cm, while Fe 2+ liberation was observed between 2 and 6 cm. Deeper Fe 2 + liberation may have occurred, but liberation results were complicated by Fe 2+ precipitation during the incubations,

As at $4, there was no evidence for dissolved sulfide-mediated Fe 2 + or Mn 2 + liberation to solution. At $9, only Mn 2 * liberation was observed from between 2 and 8 cm depth, and may have

32

D.E. C A N F I E L D E T AL.

02 (pM)

02 (I~M) 25O

0 i

-I

i

i

i

i

t

i

_2

i

50

,

I.

,

08 2

O

4

0

0 0

0 3

0 0

0

2

6

0

0

°1

0

8"

0

4

250

200

15o

,

0

O

Q

~0o ,

O O

O,

A E vE

o

O 0

I0-

0

El

12-

6

0

I

14

0

7 8

I

s.

I 0

400

-]

$9

(

18<

o

800

z,bo

d~o

O~ Consumption (nmoles cm-2 d-l) (D~DB)/Ds

O'2 Consumption (nmoles cm-2 d-l) (Ds+DB)/Ds

Fig. 5. I n situ profiles of 02 at $4 and Sg. Between 4 and 6 profiles of 02 were obtained at each site showing similar results. Modeled rates of 02 consumption with sediment depth are also shown. See text (Discussion) for details on 02 consumption calculation. NH4 ÷ Liberation (nmoles cm "a d "1)

0

30

60

90

120

150

10

20

30

40

50

60

15

30

45

60

75

90

0

2"

A I=

4"

O. G) C3

6-

o

8"

10

Fig. 6. Rates of NH2 liberation measured in the incubation experiments. Error bars represent _ 1 S . D . uncertainty in the rates as determined from statistical analysis of time vs. NH~ trends. See Canfield et al. (in press) for details.

occurred deeper, but, as at $6, mineral precipitation was observed in the deeper incubations. At $9 there was no evidence that Mn 2÷ liberation resulted from reaction between dissolved sulfide and Fe 2 ÷ or Mn oxides. Discussion Total carbon oxidation rate

Rates of 02 uptake are used to obtain depth integrated rates of carbon oxidation (referred to

here as "Total Carbon Oxidation Rate"). To accomplish this we first identify that 02 is utilized both in heterotrophic 02 respiration (hereafter referred to as 02 respiration) and to oxidize the reduced products of anaerobic organic carbon oxidation. These products include the reduced forms of the anaerobic electron acceptors (e.g., Mn 2+, Fe 2÷ and H2S), and the NH2 liberated from organic matter during anaerobic oxidation. The reduction of Fe oxides, Mn oxides and sulfate, and the subsequent oxidation of Fe 2 +, Mn 2 ÷ and H2S by 02 has the net stoichiometry of 02 respira-

33

ORGANIC CARBON OXIDATION IN CONTINENTAL MARGIN SEDIMENTS TABLE 3

Sulfate Reduction (nmoles ¢m-3 d-l) 30

0

60

I

o •6

90

I

120

I

i

150 I

180

O

02 Respiration: O

II

CH~O + O 2 ~ H 2 0 + COz Denitrification: 4/5H ÷ + C H 2 0 + 4/5NO~ ~ C O 2 + 2/5N 2 + 7/5H20 Mn reduction: 4H ÷ + C H 2 0 + 2MnO2---,2Mn 2 ÷ + 3H20 + CO 2 2H20 + 2Mn 2 ÷ + O 2~ 2MnO 2 + 4H +

2

O

)11

•

O

4 •

.,C

K

@ ,,,,.,,

Organic carbon oxidation reactions, and the subsequent oxidation of reduced species

O

CH20 + O2--*H20 + CO 2

6

•

Fe reduction: 8H ÷ + CH20 + 4 F e O O H - , 4 F e 2 + + CO 2 + 7H20 6H20 + 02 + 4Fe 2 + --*4FeOOH + 8H +

O

8 •

CH20 + O2--~H20 + CO 2

O

Sulfate reduction: H + + C H 2 0 + 1/2SO~- ~ C O 2 + 1/2H2S + n 2 0 02 + 1/2H2S--* I/2SO 2- + H +

10 Fig. 7. Rates of sulfate reduction at the different sites.

CH20

TABLE 2

+

02 "~ H 2 0

+ CO

2

NH~ oxidation: NH2 + 2 0 2 - , NO3 + H 2 0 + 2H ÷

ZCO2 and NH,~ production rates at S6 Depth (cm)

CO2 prod. NH~ prod. (nmoles c m - 3 d - 1)

0-0.5 0.5-1 1-2 2-3

347 231 351 146

(48)" (28) (89) (45)

37 47 26 20

(11) (6.0) (2.4) (3.3)

ECO2/NH, ~

9.4 4.9 13.7 7.4 Ave= 8.85

(3.1) (0.84) (3.7) (2.6) (3.7)

a( )=one S.D. uncertainty.

tion (reactions summarized in Table 3). Hence, 0 2 is taken up by a sediment in direct proportion to the total carbon oxidation rate, including carbon oxidized by both aerobic and anaerobic pathways. An exception is denitrification whose reduced product is N 2 gas which is not further involved in sedimentary redox processes, and as such, has no direct bearing on the 02 budget (Table 3). The 02 used to oxidize NH2 was not constrained in our experiments, but we assume as a reasonable estimate that the amount of NH~oxidized by 02 to NO3 was equal to the amount of NO3 used in denitrification (Table 1). Finally, some reduced species, particularly Fe 2 + and sulfide (as pyrite), are buried in sediments and not reoxi-

dized by 02. This loss of reductant, however, is not significant in Danish coastal sediments (Jergensen and Revsbech, 1989) and the effects of reduced species burial on the O2 budget will be ignored. The total organic carbon oxidation rate, then, including Oz respiration, denitrification, sulfate reduction, Fe reduction and Mn reduction is equal to the Oz flux into the sediment minus the 02 used to oxidize NH~, plus the carbon oxidized by denitrification. T f o x i d = O2Flux -- O2NHa-oxid "[- Cdeni t

(1)

where TCoxid is the total depth integrated carbon oxidation rate, O2Fi,x is the measured flux of 02 into the sediment, Cdc.it is the carbon oxidation rate by denitrification, and O2NH4.oxid is the 02 flux used to oxidize NH~- (units ofmmoles m -2 d-t). Two 02 are required to oxidize NH~- to NO3, and 4/5 NO~ oxidize one organic carbon to E C O 2 (Table 3). Assuming, as above, that the NO~ for denitrification originates from NH~" oxidation, then, 8/5 02 are used in NH~ oxidation for each

34

D.E, CANFIELD ET AL.

organic carbon oxidized by NO3. Making this substitution into Eq. 1 yields the final relationship between TCoxid, O2~lux and Cdeuit: (2)

TCoxid = O2Flu x -- 3/5Cdeni t

Total rates of carbon oxidation calculated from Eq. 2 are summarized in Table 1. Calculating total rates of carbon oxidation is the first of several steps used to determine the importance of the various electron acceptors in organic carbon oxidation. For reference, all of these steps, along with some of the major assumptions, are given in Table 4.

Rates of carbon oxidation with depth Our approach in calculating the importance of individual organic carbon oxidation pathways relies on the quantification of organic carbon oxidation with sediment depth. The preferred approach is to measure these rates directly as ECO2 production, which, unfortunately, was only

TABLE 4 Summary of steps in carbon oxidation rate calculations Step

Comments

02 uptake Total C-oxidationrate

Measured in lab From 02 uptake after adding C-oxid by denitrificationand subtracting 02 used in NH~ oxid. From NH2 liberation results Combining 02 and NO~ penetration depths with C-oxidation rate Using measured rates of denitrification Carbon oxidation below zone of 02 and nitrate penetration Using measured rates of sulfate reductioncorrected for higher metabolic activity in bag incubations From solid phase Fe, Mn, S, and incubationresults

C-oxidation rate with depth Quantify sum of 02 respiration and denitrification Separate 02 respiration from denitrification Sum of sulfate reduction, Mn reduction, and Fe reduction Separate sulfate reduction from Mn and Fe reduction Separate Mn reduction from Fe reduction

accomplished at S 6. We have, however, measured rates at all sites and assume that these are a reasonable proxy indicator of organic carbon oxidation rates. The fact that ECO2 and NH2 were liberated to solution at $6 in a ratio of 8.85 + 3.7 (Table 2), typical for continental margin sediments (Canfield et al., in press), lends support to this assumption. We further assume that organic carbon oxidation rates in surface sediments normally containing 02 and NO 3 were unaffected by the complete removal of these species during the early stages of our incubations. This assumption gains support from the observation that relatively fresh organic matter is oxidized at similar rates in the presence and absence of 02 (e.g., Westrich and Berner, 1984). With these assumptions, NH~ liberation rates are summed (Fig. 6), and the fraction of the total NH~ liberation contributed by each layer is calculated. This, then, is also the fraction of the total carbon oxidation contributed by each layer. The actual carbon oxidation rate is the product of the fraction of total carbon oxidized in the layer and the total carbon oxidation rate (Table 1). Results are given in Fig. 8, and the rates will be termed "C-oxid". For comparison, rates of carbon oxidation by sulfate reduction (all sites), and ECOz liberation (at $6) as measured in the sediment incubations are also presented in Fig. 8. At $6, measured rates of ECO2 production are twice as great as C-oxid. At Sa, rates of carbon oxidation by sulfate reduction exceed by about a factor of two C-oxid at depths below 4 cm. A comparison is not possible at $9 since ECO2 production was not measured and sulfate reduction was a very minor process (Fig. 7). However, the discrepancies between C-oxid (calculated ultimately from 02 uptake rates) and measured rates (from incubation experiments) imply that bacterial activity in the incubations was greater than in the 02 uptake experiments, with two possible causes. First, sediment incubations were performed at a somewhat higher temperature (2-3°C) than the 02 uptake experiments, the higher temperature likely stimulating metabolic activity. Second, the decomposition of macrofauna entombed in the incubation containers could have enhanced the carbon oxidation rate.

NH~- liberation

ORGANIC CARBON OXIDATION IN CONTINENTAL

MARGIN

35

SEDIMENTS

Carbon Oxidation (nmolea cm-3 d-l) 0 00

100 i

,

l

200 ,

l

,

300 i

4~

500

100

200

Oo

O

300

400

100

200

300

•

) 2" O

O

O

4"

o =. D. ¢D Pt

Ss

$4

10 ¸

-0- c-ox~ • M4mm co$~prod 0 C-ox~SRed

Fig. 8. Rates of organic carbon oxidation with depth at the three sites, as determined by combining total organic carbon oxidation rates (Table 1) with relative rates of NH~ liberation from the sediment incubations (Fig. 6). See text for calculation details. Also included are rates of carbon oxidation from sulfate reduction, and measured rates of Y-CO= production at $6.

To calibrate experimental results, rates of ~ , C O 2 production and carbon oxidation by sulfate reduction at $6 are reduced by a factor of two. These new rates are compared with C-oxid in Fig. 9. Canfield et al. (in press) have shown that carbon

oxidation below 4 cm at $4 is dominated by sulfate reduction. Hence, measured rates of sulfate reduction are similarly reduced by a factor of 2 to be comparable with C-oxid as calculated above (Fig. 9).

Carbon Oxldatlon(nmolescm-3d-1) 0

o ?:.::

100

200

300

. . . . . . . .

400

500

1O0

200

300

1O0 i

200 i

300

2"

1

• ......

C-ox~ I

s n ~ co.

Fig. 9. Rates of carbon oxidation as in Fig. 8, with corrected ZCO2 liberation (at S6) and carbon from sulfate reduction. See text for details of correction justification and procedure. Included on the figure are depths of 02 and nitrate penetration (horizontal dashed lines). The area above the dashed line represents the sum of carbon oxidation by 02 respiration and denitrification. Hatched area represents carbon oxidation by metal oxide reduction (Fe reduction and Mn reduction).

36

D.E. CANFIELDET AL.

Importance of &dividual carbon oxidation pathways The importance of the different carbon oxidation pathways is determined by first identifying in which sediment level each oxidation processes was active, and then calculating rates from the carbon oxidation rates in Fig. 9. To begin, at all sites, 02 and nitrate penetrated to similar depths (compare Figs. 3 and 5). Assuming that 02 respiration and denitrification were restricted to the region containing measurable O2 and nitrate, these two processes were thus confined to the upper 0.7cm at $4, 1.3 cm at $6, and 2.0 cm at $9 (depths marked on Fig. 9). Rates of carbon oxidation, then, by the sum of 02 respiration and denitrification are the integrated rates of carbon oxidation to the above depths, minus carbon oxidation by additional anaerobic processes. We assume no Fe or Mn reduction in the region containing 02 and NO3. Thus, with little or no sulfate reduction (Fig. 7), organic carbon oxidation by O2 and NO£ at $4, $6, and $9 are respectively, 2.61, 2.12, and 1.03 mmoles m -2 d -1. It is important that these values depend only on TCo~id (Eq. 1), the relative rates of carbon oxidation with depth, and the depths of O2 and NO3 penetration, but not on the mismatch in rates between sediment incubations and O2 uptake measurements. Carbon oxidation by 02 respiration is obtained by subtracting carbon oxidation by denitrification (Table 1) from these values with results summarized in Table 5. Below the zone of O2 and NO 3 penetration, carbon oxidation occurs only by sulfate reduction, Fe reduction and Mn reduction. The amount of

TABLE 5 Importance of different carbon oxidation pathways Pathway

$4 $6 C-oxid Rate a C-oxid Rate

$9 C-oxid Rate

O2 respiration Denitrification Mn reduction Fe reduction SO2- reduction

2.11 0.5 0.0 5.1 8.1

0.4 (3.6) 0.63 (5.7) 9.9 (90.7) 0.0 (0.0) <0.1 (< 1.0)

(13.6) b (3.2) (0.0) (32.1) (51.1)

1.74 (17.4) 0.38 (3.8) 0.0 (0.0) 5.2 (50.9) 2.9 (27.9)

"Rate of organic carbon oxidation (mmoles m-2 d-1). b% total organic carbon oxidation by each pathway.

carbon oxidation by sulfate reduction is obtained from the corrected sulfate reduction rate measurements in Fig. 9, with results compiled in Table 5. Rates of carbon oxidation by metal oxide reduction (both Fe oxide and Mn oxide) are obtained as the difference between the carbon oxidized by sulfate reduction and C-oxid (hatched area in Fig. 9). The relative importance of sulfate reduction vs. metal oxide reduction is to some extent dependent on the accuracy of the correction factors used to calibrate measured rates of sulfate reduction. If the correction factors are too high, then sulfate reduction has been underestimated and metal oxide reduction is less important than in Table 5. If the correction factors are too low then sulfate reduction would be less, leaving more carbon oxidation by metal oxide reduction. However, using an independent procedure applied only to the incubation results, Canfield et al. (in press) have found sulfate reduction and metal oxide reduction to be of a similar relative importance. To quantify separately rates of Mn reduction and Fe reduction, total metal oxide reduction rates (Fig. 9) are combined with incubation results and solid phase distributions. At $9, virtually no sulfate reduction was measured (Fig. 7), incubations gave no evidence for Fe reduction, and abundant Mn oxides were available for reduction (Fig. 4). At this site, then, Mn reduction was the only important anaerobic carbon oxidation process. Incubation experiments showed Mn 2÷ liberation in the 0.5-1 cm interval at $4 (ignoring Mn 2+ liberation between 0 and 0.5 cm, see above) and in the 1-2 cm interval at $6. High concentrations of Mn oxides were also found in these intervals potentially supporting dissimilatory Mn reduction (Fig. 4). We note however, that solid phase profles also demonstrate the mixing of Mn oxides and acid volatile sulfide (AVS) by bioturbating organisms into a common "reaction" zone located at about 1 cm depth at $4 and 2 cm at $6 (Fig. 4). Aller and Rude (1988) have argued that AVS and Mn oxides readily react in sediments: FeS + 7H + + 9/2MNO2 ~ FeOOH + SO 2- + 9/2Mn 2 + + 3H20

(3)

From Eq. 3, if the Mn oxide gradient is less than

ORGANIC CARBON OXIDATION IN CONTINENTAL MARGIN SEDIMENTS

to 4.5 times the sulfide gradient, then AVS will be supplied in excess of that required to completely reduce the oxides. At $4 and $6, the Mn oxide gradient is respectively 0.87 times and 3.16 times the AVS gradient; in both cases an excess supply of AVS is indicated (Canfield et al., in press). At these two sites then, Mn reduction may mostly, or even completely, result from reaction with AVS, with no substantial evidence for the dissimilatory reduction of Mn oxides. Accordingly, without more support for dissimilatory Mn oxide reduction, we have assumed dissimilatory Fe oxide reduction as the only metal oxide reduction process at $4 and $6 (Table 5). Assuming that we have underestimated the importance of Mn reduction, and that it accounts for all of the carbon oxidation between 0.5 and 1 cm at S,, and 1 and 2 cm at $6, only 7% and 10% of the total carbon oxidation, respectively, could be by dissimilatory Mn oxide reduction (see Canfield et al., in press). General discussion and implications

From the summary of carbon oxidation pathways in Table 5, several interesting conclusions emerge. First, and perhaps most surprising, is that although 02 uptake is good indicator of organic carbon oxidation rate (Table 1), only between 3.6 and 17.4% of the 02 is used directly in the oxidation of organic carbon. 02 respiration will be an even smaller percentage of total sediment respiration if rates of anaerobic carbon oxidation below 10 cm are included. The basic reason for these relatively low rates is that 02 respiration can only occur where 02 is present, and for the sediments studied here, that region accounts for a variable, but relatively small percentage of the total sediment metabolism. We suspect that 02 respiration will prove to be a relatively minor process of organic carbon oxidation in many continental margin sediments, where considerable sediment respiration continues below the zone of 02 penetration. It may be argued that burrowing organisms occasionally deliver 0 2 to greater depths than measured with our electrodes. Although this is likely true, we have rarely observed such events in numerous in situ and lab 02 profiles at these sites, and conclude that they must not be a signifi-

37

cant transport pathway for 02 into the sediment. In other sedimentary environments deep 0 2 transport by infauna may be more significant, and intensive 02 microprofiling could be used to address this. As mentioned, 02 and nitrate penetrated to similar depths in all three of these sediments (Figs. 3 and 5). If denitrification does not occur in the presence 02 (Sorensen et al., 1984), then it must have been restricted to a narrow zone just below the zone of 02 penetration. Overall, denitrification accounted for between only 3.2% to 5.7% of the total carbon metabolism (Table 5). In other studies of continental margin sediments, denitrification was responsible for a similar relatively small percentage of the total carbon oxidized (S~rensen et al., 1979; Jorgensen, 1983). An exception is the study of Devol (1991) who found that up to 30% of the benthic respiration in sediments of the Washington coast was by denitrification. Also, from the results of Jahnke et al. (1990) and Jorgensen and Sorensen (1985) (see Canfield, 1993), when the concentration ratio of NO3/O2 in water overlying a sediment becomes greater than about 2, denitrification may dominate benthic carbon oxidation. A significant result of the present study is that metal oxide reduction was very important, accounting for about 30% of the carbon oxidation at $4, 50% at $6, and 90% at $9 (Table 5). Aller (1990) reported than Mn reduction was responsible for nearly all of the organic carbon oxidation in sediments of the Panama Basin, which have somewhat higher Mn oxide levels than $9. Also, S~rensen and J~rgensen (1987), and Hines et al. (1991) have argued that both Mn and Fe reduction may play a significant role in carbon oxidation in coastal sediments, though they were not able to quantify the importance. Taken together, all of these studies suggest that metal oxide reduction is likely more significant than previously thought (e.g., Henrichs and Reeburgh, 1987). Both Aller (1990) and Canfield et al. (in press) have stressed that significant dissimilatory metal oxide reduction requires the rapid mixing by infaunal organisms of metal oxide species into the sediment to be reduced, and reduced species upwards to be reoxidized. Such a scenario is

38

D.E. CANFIELD ET AL.

indicated by the nearly equal, but opposite gradients in solid phase Fe 2 + and Fe 3 ÷ at $4 and S6. At $9, the gradient of solid Mn 4+ into the sediment is much steeper than solid Mn 2 ÷ to the sediment surface. At this site most of the Mn 2 + is delivered to the sediment surface by dissolved species transport (probably enhanced by bioirrigation), as evidenced by the steep concentration gradient in dissolved Mn 2 ÷ (Fig. 3). Canfield et al. (in press) have argued that if mixing of the solid phase can be approximated by a diffusional process, then a diffusion coefficient (DB) can be determined to balance the measured metal oxide concentration gradient (dC/dx) with rates of metal oxide reduction (Table 5). The expression is given by Fick's first law: Rate = -

DBdC/dx

(4)

Biodiffusion coefficients are summarized in Table 6 and are within the range reported for continental margin sediments (Van Cappellen et al., 1993). The DB values in Table 6 are, however, about 1/2 as great as those reported by Canfield et al. (in press), consistent with the lower TCoxid used in the present calculations.

Fate of 02 If 02 is not used primarily in carbon oxidation, then most must be used to oxidize the reduced products of other carbon oxidation reactions (Table 3). The influence of reduced species oxidation on the 02 budget of coastal sediments was first recognized by Jargensen (1977, 1982), who calculated that much more sulfide was produced in sediments than was buried as pyrite. This additional sulfide production must have been oxidized TABLE 6 B i o d i f f u s i o n coefficients (DB) to s u p p o r t m e t a l o x i d e r e d u c tion rates Site - - m e t a l

DB ( c m 2 y r - 1)

$4 - - F e 3 + S6 - - F e a÷ S9 - - M n 4÷

80 87 19

by 02, consuming about 50% of the 02 flUX,and leaving about 50% for 02 respiration (Jargensen 1977, 1982). Our results indicate even less significant 02 respiration, consistent with the additional consumption of 02 by Fe 2 + and Mn 2 + oxidation. The fate of 02 may also be illuminated by analyzing directly the sediment profiles of 02. For this analysis the in situ profiles for $4 and $9 will be used (Fig. 5). Basic mass balance constraints require that at steady state, a change in the flux of a chemical species with depth indicates that either consumption or production of the species has occurred, and the rate of change of the flux is a measure of the consumption or production rate. Hence, a decreasing 02 flux with depth requires that 02 consumption has occurred. The flux at a given depth is given by Fick's first law, and the rate of change of the flux with depth, which is equivalent to the consumption rate, is determined by analyzing the flux in adjacent levels in the sediment: [(D~ +

Ds)/D,][Rate = ~Ds!(dCdd~Ca/dx)]l k x._b A (5)

At lim A x e 0 this expression is the 2nd derivative of the 02 profile, where Rate is the 02 consumption rate (nmoles cm -a d-1), dCa/dx and dCb/dx (nmoles cm -4) are 02 concentration gradients in adjacent layers separated by a distance AXa_b (cm), and Ds is the sediment diffusion coefficient for O2 (cm 2 d -t) at 7°C which has been corrected for porosity ~ (Iversen and Jorgensen, 1993). The term (D8 + Ds)/Ds augments the calculated 02 consumption rate for enhanced 02 transport by bioirrigation (Da, cm 2 d -t) assuming that the transport may be modeled as a diffusional process. Using Eq. 5, 02 consumption rates have been calculated from the in situ 02 profiles and are presented with the profiles in Fig. 5. The rates have not been corrected for enhanced diffusion by bioirrigation as the depth distribution of 02 consumption is of the most interest here. At $4, very little if any O2 consumption is indicated by the 02 profile in the surface 3 mm of the sediment. The most vigorous 02 consumption is observed near the oxic-anoxic interface where the oxidation of

39

ORGANIC CARBON OXIDATION 1N CONTINENTAL MARGIN SEDIMENTS

reduced species is likely. Hence, the oxidation of reduced species, diffused and mixed from below, is indicated as the most important sink for 02. A similar situation was found during the spring and summer months in Arhus Bight by Rasmussen and J~rgensen (1992). At $9, the distribution of 02 consumption is quite different. The most rapid 02 consumption occurs in the surface 6 mm, and is relatively uniform at somewhat lower rates below. High rates of 02 consumption are well separated from the oxic-anoxic boundary indicating that 02 respiration may be an important sink for 02, inconsistent with the mass balance results (Table 5). We offer two explanations for this inconsistency. First, Canfield et al. (in press) demonstrated that reduced Mn 2÷ adsorbed very strongly onto oxidized surface sediment at $9. They speculated that dissolved Mn 2+, diffusing from below, may adsorb onto sediment particles to be mixed and oxidized throughout the aerobic zone. This could account for the lack of localized, enhanced, 02 consumption at the oxic-anoxic boundary. As another possibility, the surface NH~- production rates at $9 were much lower than might have been expected (Fig. 6). If NH~ was very strongly adsorbed in this region, or involved in yet unknown secondary redox reactions, the NH2 production rate would have underestimated rates of organic carbon oxidation. If this were the case, then a higher percentage of the total carbon oxidation would have occurred in the O2-containing region, and rates of 02 respiration would have been higher than calculated. We can resolve this issue only with further study.

Conclusions We have incorporated a variety of different rate measurements to determine the importance of 02 respiration, Fe reduction, Mn reduction, denitrification and sulfate reduction in carbon oxidation for three continental margin sediments. Overall, anaerobic processes dominated the oxidation of organic carbon, and at $9, which had surface Mn concentrations of 3 to 4 wt%, Mn reduction was the only significant anaerobic carbon oxidation pathway. At $4 and $6 both sulfate reduction and Fe reduction accounted for most of the organic

carbon oxidation, with sulfate reduction most important at $4, and Fe reduction dominating at $6.02 respiration accounted only between 3.6 and 17.4% of the organic carbon oxidation, a surprisingly small percentage compared to previous estimates in other coastal sediments. In the sediments studied here, the depths over which 02 was measured were responsible for only a relatively small percent of the total sediment metabolism; this is the basis for our low calculated rates. 02 respiration should prove to be a relatively minor processes in other sediments where considerable carbon oxidation occurs below the zone containing 02. We also suspect that further study will reveal Fe and Mn reduction to be more significant in coastal sediments than previously thought.

Acknowledgments We thank first the captain and crew of the Gunnar Thorson for a most enjoyable and productive cruise. We thank also Preben Sorensen, Dorthe Thomsen, and Anders Tengberg for their assistance. Very helpful reviews by Rick Jahnke, Ellery Ingall and Henry Blackburn are also greatly appreciated. Financial support provided by the Danish Agency of Environmental Protection through Marine Research Program 90, with partial support by NASA (NAGW-3117 to DEC).

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