Journal of Marine Research, 63, 457– 469, 2005
Similar rapid response to phytodetritus deposition in
shallow and deep-sea sediments
by L. Moodley1,2, J. J. Middelburg1, K. Soetaert1, H. T. S. Boschker1,
P. M. J. Herman1 and C. H. R. Heip1
ABSTRACT
The short-term benthic response to an input of fresh organic matter was examined in vastly
contrasting benthic environments (estuarine intertidal to deep-sea) using 13C-labeled diatoms as a
tracer of labile carbon. Benthic processing was assessed in major compartments through 13Cenrichment in ⌺CO2, in bacteria-specific phospholipids and in fauna tissue. A rapid response was
evident in all environments. Under warm bottom water (14 –18°C), similar quantities of the added
carbon were respired within 24 hours in shallow and deep-sea sediments. However, the speed and
magnitude of respiration were strongly reduced under low bottom water temperature (4 – 6°C), both
in a shallow and a deep-sea site. Rapid carbon respiration even in deep-sea sediments almost devoid
of fauna highlights the key role of bacteria, the most ubiquitous benthic component, in this short-term
respiration of fresh organic matter. However, when present, fauna rapidly ingest algal material,
thereby increasing the amount of carbon processed and directly extending carbon flow pathways.
1. Introduction
Sediment communities play a major role in oceanic carbon cycling as they ultimately
determine the fate of organic carbon that has escaped water column degradation. It is well
established that relatively fresh material, termed phytodetritus, is deposited seasonally or
episodically in many places on the ocean floor including the deep-sea (see review by
Gooday, 2002). Although the benthic response to deposition of organic matter (OM) may
be rapid, also in deep-sea sediments, this is not always evident. Carbon processing may
proceed by respiration and uptake by the different biotic components. Field observations
on deep-sea short-term benthic response in terms of respiration of the OM deposit,
followed through sediment community oxygen consumption (SCOC), are often contradictory (see review by Beaulieu, 2002). Moreover, knowledge of the controlling factors,
especially the impact of the structure of the sediment biota is limited.
It is currently not possible to follow a naturally occurring parcel of organic matter but the
addition of an external carbon source offers the opportunity of studying the dynamics of
1. Department of Ecosystem Studies, Netherlands Institute of Ecology (NIOO-KNAW), Korringaweg 7, 4401
NT Yerseke, The Netherlands.
2. Corresponding author. email: [email protected]
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the benthic response. The use of 13C-enriched algal carbon as a tracer of labile carbon
(Blair et al., 1996) has proven to be a powerful tool to follow the fate of fresh organic
matter entering the sediments. The label can be traced in different benthic components
including respiration (directly through 13C-enrichment in ⌺CO2 (Blair et al., 1996)) and
bacteria (through 13C-enrichment in bacteria-specific phospholipids (Boschker and Middelburg, 2002)). As in earlier tracer experiments (e.g. Cahet and Sibuet, 1986; Boetius and
Lochte, 1996; Relexans et al., 1996), 13C-labeled algal carbon enrichments revealed that
benthic processing might be rapid in deep-sea sediments (Blair et al., 1996, 2001; Levin et
al., 1997, 1999; Moodley et al., 2002; Witte et al., 2003a,b). However, it remains unclear
how oceanic environments compare in terms of speed and magnitude of the benthic
response. Comparisons of the limited number of quantitative tracer studies are complicated
by a number of factors. First of all, there are differences in the benthic components that
were quantified; for instance, only few investigations traced the fate of tracer carbon into
the inorganic compounds (⌺CO2, Blair et al., 1996; Moodley et al., 2002). Secondly,
slightly different ways of preparation of the algal carbon may affect the state of the carbon
and subsequently its short-term degradability. Thirdly, the quantity of algae administered
is not always the same. Not only can this have an effect on the amount of carbon taken up
or respired, but also there is experimental evidence that carbon turnover rates strongly
relate to the amount of carbon added (e.g. Osinga et al., 1995). Finally, although it has been
suggested that both biotic biomass and temperature could affect the benthic response, these
two factors were not always independent in previous studies. Therefore, it is not clear
whether the low short-term carbon turnover rates observed in certain deep-sea sediments
are a result of low benthic biomass (as suggested by Witte et al., 2003b) or a combination
of low biomass and low temperature (Moodley et al., 2002).
In order to gain insight into the factors that control sediment response to fresh OM input,
we examined the short-term benthic processing of algal carbon at seven contrasting sites
(estuarine intertidal to oligotrophic eastern Mediterranean deep-sea sediments) that differed strongly in sediment trophic status (as reflected in surface sediment background
carbon mineralization rates and benthic biomass standing stock). Carbon deposition events
were mimicked by adding a fixed quantity of 13C-labeled diatoms, prepared in the same
way, to undisturbed sediment cores maintained for 24 hours at in situ bottom water
temperature (4 –18°C). The impact of temperature was further examined by experimentally
lowering the temperature at a shallow site (from 16 to 6°C). Carbon processing was
followed through 13C-enrichment in ⌺CO2 in the overlying water, in surface sediment
bacteria-specific phospholipids and fauna tissue (macro- and meiofauna including foraminifera).
2. Material and methods
Incubations were done with undisturbed multicore (i.d. 9.5 cm) sediment samples
shipboard in a temperature-controlled container except for the estuarine sediments that
were collected by hand at low tide and incubated in the laboratory at ambient temperature
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Moodley et al.: Benthic rapid response to phytodetritus deposition
459
(Table 1). Cores had about 20 cm sediment and 1.5 liter ambient bottom water and were
aerated until initiation of the experiment (within 5–10 hrs) and remained oxic during the
experiment. Axenic, freeze dried 21.5% 13C-enriched Skeletonema costatum (cultured and
concentrated as described in Moodley et al., 2002) was used as a tracer of fresh organic
matter of which 36 mmol C m⫺2 was added to the cores. Diatoms, resuspended in
0.2-␮m-filtered seawater, were carefully brought evenly onto the surface of the sediment
with a long pipette. This addition represented 0.7–2.7% of the natural particulate organic
matter in the 0 –1 cm interval of the sediment (Table 1). Cores were sealed off with lids
equipped with a magnetic stirrer and incubated in the dark. At different time intervals,
10 ml of overlying water was sampled for ⌺CO2 through a tygon tube in the lid by
displacement following depression of the O-ring fitted lid. Water samples collected in glass
vials were immediately sealed with aluminum caps fitted with rubber septa. A headspace
was created by injecting 3 ml of nitrogen and the sample was then acidified and stored
upside down in the fridge until analyzed. After 24 hours, the overlying water was carefully
removed and the upper cm of the sediment was sliced off and sampled for different biotic
components.
Sediment was gently homogenized from which 3 ml was taken for analysis of bacteria
carbon uptake through PLFA (polar lipid derived fatty acids), 10 ml for meiofauna taxa
⬎63 ␮m and the rest for macrofauna taxa ⬎300 ␮m. All samples were frozen and
processed in the laboratory as described in Moodley et al. (2002). Carbon-isotopic analyses
of PLFA’s were done according to Boschker et al. (1999) and Middelburg et al. (2000).
Details of the measurement of ␦13-⌺CO2 and ␦13Corg of faunal compartments are given in
Moodley et al. (2000). Carbon isotopes are expressed in the delta notation (␦13C) relative
to Vienna Pee Dee Belemnite (VPDB): ␦13C ⫽ ((13C/12C)sample/(13C/12C)ref ⫺ 1)*1000.
Incorporation of 13C is reflected as excess (above background) 13C and is expressed in
terms of specific uptake (i.e. ⌬␦13C ⫽ ␦13Csample ⫺ ␦13Cbackground) as well as total uptake
(I). Specific uptake is a qualitative measure of 13C-uptake, with ⌬␦13C ⬎ 0 ⫽ 13C-uptake.
Total uptake is a quantitative measure of 13C-uptake and is calculated as the product of
excess 13C (E) and biomass of the consumers or concentration of CO2. Excess (E) 13C is
the difference between the fraction 13C of the background (Fbackground) and the samples
(Fsample): E ⫽ Fsample ⫺ Fbackground where F ⫽ 13C/(13C ⫹ 12C) ⫽ R/(R ⫹ 1). The carbon
isotope ratio (R) was derived from the measured ␦13C values as: R ⫽ (␦13C/1000 ⫹ 1) ⫻
RVPDB, with RVPDB ⫽ 0.0112372. For the Fbackground of CO2, we did not use ambient
␦13-⌺CO2 but that of water samples taken from experimental cores at the beginning of the
incubation thereby correcting for any contamination of 13C-bicarbonate in the added
diatoms. Fbackground of fauna was measured in specimens isolated from a separate
multicore. We calculated the biomass (organic carbon content) of the different faunal
groups directly from the area counts given in the standard output of the isotope ratio mass
spectrometer calibrated with glucose (0 –120 ␮g C, r 2 ⫽ 0.99). Bacterial data are based
on the concentrations and 13C content of bacteria-specific biomarkers (i14:0, i15:0, a15:0,
i16:0) assuming bacterial biomarkers ⫽ 14% of total bacterial PLFA’s (calculated from
51°26⬘ N
3°.57⬘ E
53°42⬘ N
4°.32⬘ E
39°47⬘ N
25°32⬘ E
40°19⬘ N
25°11⬘ E
35°40⬘ N
26°35⬘ E
35°20⬘ N
28°44⬘ E
42°38⬘ N
10°00⬘ W
St. 1
Estuary
St. 2
North Sea
St. 3
N. Aegean
St. 4
N. Aegean
St. 5
E. Med.
St. 6
E. Med.
NE Atlantic
07-1999
intertidal
07-2000
37
08-1999
102
08-1999
698
08-1999
1552
08-1999
3859
05-1999
2170
Date & depth
Bkgrd C-mineral.
9.27 ⫾ 1.27
4.51 ⫾ 0.72
(2.12 ⫾ 0.73)
1.11 ⫾ 0.10
0.11 ⫾ 0.10
0.01 ⫾ 0.01
0.05 ⫾ 0.02
0.22 ⫾ 0.06
Corg content
5.5 ⫾ 0.4
4.3 ⫾ 0.0
2.6 ⫾ 0.1
1.7 ⫾ 0.0
1.5 ⫾ 0.2
1.4 ⫾ 0.1
2.8 ⫾ 0.4
18
16
(6)
14
14
14
14
4
BW temp
*Macro- and meiofauna including foraminifera.
Position
Station
11.5 ⫾ 0.6
0.3 ⫾ 0.2
0.5 ⫾ 0.2
3.1 ⫾ 0.2
61.0 ⫾ 50.7
(63.2 ⫾ 12.8)
6.1 ⫾ 1.5
112.5 ⫾ 20.8
Fauna*
Bacteria
26.1 ⫾ 4.0
26.0 ⫾ 8.8
21.2 ⫾ 0.0
30.5 ⫾ 2.4
192.2 ⫾ 16.8
(224 ⫾ 34.0)
43.5 ⫾ 21.3
104.9 ⫾ 4.9
Biomass
0.01 ⫾ 0.00
⬍0.01
⬍0.01
0.02 ⫾ 0.01
0.41 ⫾ 0.16
(0.04 ⫾ 0.01)
0.05 ⫾ 0.00
1.37 ⫾ 0.04
Fauna*
0.05 ⫾ 0.00
0.22 ⫾ 0.12
0.15 ⫾ 0.02
0.34 ⫾ 0.08
0.74 ⫾ 0.18
(0.23 ⫾ 0.02)
0.31 ⫾ 0.16
0.95 ⫾ 0.54
Bacteria
C-Uptake
0.60 ⫾ 0.02
4.99 ⫾ 0.63
5.50 ⫾ 0.59
6.22 ⫾ 0.50
6.05 ⫾ 0.30
(1.20 ⫾ 0.26)
5.79 ⫾ 0.23
5.09 ⫾ 0.18
Respiration
Table 1. Location of stations. Date of sampling, water depth (m) and bottom water (BW) temperature (°C). Surface sediment (0 –1 cm) organic
carbon content (Corg, mol C m⫺2), background carbon mineralization rates (mmol C m⫺2 day⫺1), biota biomass and algal carbon uptake
(mmol C m⫺2). n ⫽ 2 ⫾ s.e.
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Moodley et al.: Benthic rapid response to phytodetritus deposition
461
literature data given in Middelburg et al., 2000) and 0.056 gC PLFA/gC biomass
(Brinch-Iversen and King, 1990). Finally, the uptake of total added algal carbon (12C ⫹
13
C) was calculated as the quotient of total uptake (I) and the fractional abundance of 13C
in the algae (0.215). Although faunal components were analyzed separately for their 13C
uptake (Moodley et al., 2002), they are discussed in this paper as total faunal uptake in
comparison to bacteria, the most ubiquitous and expected key player (e.g. Rowe et al.,
1991; Relexans et al., 1996; Turley, 2000).
Because bulk sediment organic-carbon content is generally an unsuitable measure of
labile organic matter as it mainly depends on sediment structure, we used both background
carbon mineralization rates and biota biomass as indicators of trophic conditions. Carbon
mineralization rates are ultimately controlled by organic matter supply and biota biomass
reflects average carbon input (e.g. Soetaert et al., 1997; Moodley et al., 1998). In this study,
background carbon mineralization rate measurements were restricted to the upper cm of
the sediment and as such are an elegant tool to compare the different settings but by no
means reflect in situ total benthic activity. Background carbon mineralization rates were
calculated from CO2 production rates in sediment-water slurry incubations. A volume of
approximately 10 ml surface sediment was used for the slurry incubations, which was
directly transferred into 80 ml glass incubation bottles, diluted with 10 ml filtered seawater
(0.2 ␮m) and sealed with screw caps fitted with rubber septa. Slurries were then thoroughly
mixed (vigorously hand shaken) and purged for 5 minutes with N2:O2 (80:20) to obtain full
oxic conditions. All slurries and controls (containing only water) were incubated in the
dark at ambient temperature for 21 to 80 days (long incubations were needed for sediments
from the oligotrophic eastern Mediterranean sediments). The amount of CO2 produced was
calculated from the concentration of ⌺CO2 minus the ⌺CO2 initially present in the
pore-water and added water as described in Dauwe et al. (2001) and corrected for the
water-only respiration. All error terms presented in the text are standard errors.
3. Results and discussion
In this cross system comparison, the sites with warm bottom water (stations 1– 6,
14 –18°C bottom water temperature) covered a large gradient in water depth (estuarine
intertidal to 3859 m, Table 1) and differed vastly in trophic status, as reflected in the upper
cm sediment background carbon mineralization rates (0.01–9.27 mmol C m⫺2 day⫺1) and
benthic biomass (biomass in the upper cm ranged from 22–253 mmol C m⫺2, Table 1).
Although not designed for a detailed study of distribution biology, which would obviously
require larger samples both in terms of size and replication, the observed trends in trophic
status are in accordance with overall water depth related patterns in benthic activity and
biomass (e.g. Danovaro et al., 1999; Flach et al., 2002). Although there was a strong
gradient in fauna biomass with Mediterranean oligotrophic deep-sea sediments almost
devoid of fauna, bacteria were always present with comparable biomass except for higher
values at the two shallow, relatively eutrophic stations (1 & 2, Table 1, Fig. 1a).
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Figure 1. (a) Contribution of fauna (macro- and meiofauna including foraminifera) and bacteria to
average biomass in the upper cm at the different stations in the eastern Mediterranean, in the North
Aegean Sea, in the southern North Sea, and in an estuary in SW Netherlands. (a⬘) Biomass in cores
of station 2 maintained at low temperature and in a deep-sea site in NE Atlantic. (a) The amount of
phytodetritus processed in 24 hrs (contribution of respiration, bacterial assimilation and fauna
uptake in the top cm). (b⬘) Effect of lowering bottom water temperature at site 2, and a deep-sea
benthic response in northeast Atlantic (4°C).
Consequently, sediment samples differed strongly in sediment community structure (ratio
of bacteria to fauna biomass ranged from 1– 87, Fig. 1a).
Irrespective, within 1 day, a similar quantity of the added carbon was respired in all these
sediments (5.0 – 6.2 mmol C m⫺2, ⬃15%, Fig. 1b). This uncoupling between initial
remineralization of the added carbon and community size and structure implies that, under
warm bottom water, the short-term benthic respiration was governed primarily by the
quantity and quality of the carbon input. However, compared to this response, strongly
reduced values of respiration were observed when bottom-water temperatures were lower.
Respiration at a slope station in the NE Atlantic (2170 m, temperature 4°C) was slower and
limited compared to that recorded in sediments from the deep-sea sites (1552 and 3859 m,
temperature of 14°C) in the eastern Mediterranean (⬃5 mmol C m⫺2 at Mediterranean
stations 5 and 6 and 0.6 mmol C m⫺2 in NE Atlantic, Fig. 1 and Fig. 2). To further examine
the direct effect of temperature, temperature was experimentally lowered from 16°C to 6°C
at shallow station 2 (i.e. same community but different temperature) and this caused a
strong decrease in the speed and magnitude of respiration from 6.1 to 1.2 mmol C m⫺2 in
24 hours (Table 1 and Fig. 2), corresponding to a Q 10 of ⬃5. This is much higher than the
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Moodley et al.: Benthic rapid response to phytodetritus deposition
463
Figure 2. Dynamics of the short-term respiration. On the left y-axis ⌬␦13-⌺CO2 (open symbols) with
values ⬎0 indicating respiration of the added carbon and on the right y-axis the amount respired in
24 hrs (closed symbols). (c) Effect of lowering bottom water temperature. (d) Comparison of
deep-sea benthic response in eastern Mediterranean (14°C) and northeast Atlantic (4°C). Values
for the in situ experiment in NE Atlantic with ⬃50% lower carbon load were calculated from
Moodley et al. (2002).
Q 10 of ⬃2 derived from background carbon mineralization rates (Table 1) and may be
related to differences in OM reactivity between the resident and administered carbon (e.g.
Westrich and Berner, 1988; Middelburg et al., 1996). Evidently, temperature is a prime
factor controlling respiration in benthic ecosystems (Westrich and Berner, 1988), consistent with the overall regulatory capacity of temperature established for the pelagic
compartment of the oceans (e.g. Rivkin and Legendre, 2001). Therefore, temperature
through its direct control on metabolism (Gillooly et al., 2001), may explain these
differences in the speed and magnitude of short-term benthic respiration of fresh organic
matter. Subsurface respiration was not measured, but given that 13C-⌺CO2 accumulation in
porewater is generally a small fraction of that recorded in the overlying water (e.g.
Kristensen et al., 1992; author’s own observation in subsequent experiments), it is not
expected to alter the large-scale patterns observed in these 24-hour incubations.
Although on-deck incubations ensure accurate addition of the labeled carbon and intact
sediment recovery after incubation, there is always the concern about incubating deep-sea
sediments at 1 atmosphere. The deep-sea sediments were incubated onboard ship, but we
do not believe that this invalidates the observed trends. Firstly, an absence of or
comparable retarded response in all deep-sea sediments could in fact reflect methodological artifacts. However, there were rapid responses and they differed significantly between
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cold and warm deep-sea settings (Table 1 and Fig. 2). Secondly, and most important, this
strong contrast between the NE Atlantic and the eastern Mediterranean was also evident in
independent deep-sea in situ incubations using similar quantities of the same carbon
source. In an in situ incubation in the NE Atlantic, benthic respiration was also slow and
limited. Similar to our on-deck incubations, approximately 1% of the added carbon
respired in 24 hours (Moodley et al., 2002, see also Fig. 2d). In contrast, approximately
14% of the added carbon was respired within 24 hours in an in situ incubation at a deep-sea
site in the eastern Mediterranean (Buhring et al., in prep.), again similar to our on-deck
incubations (15%, Table 1). Finally, although on-deck incubations may underestimate
somewhat in situ rates of carbon processing (e.g. Cahet et al., 1990), this would not alter
our main conclusion: rapid benthic response both in shallow and deep-sea sediments and
that temperature is a prime factor controlling the speed and magnitude of benthic
respiration of fresh OM.
Although there was limited control of community size and structure on the short-term
respiration of the added carbon under warm conditions (Fig. 1), this may be different under
low bottom water temperature: respiration at station 2 with a higher biomass (Table 1)
maintained under low temperature was quicker and approximately twice that measured in
cold deep-sea sediment in the NE Atlantic (Table 1, Fig. 2). Additionally, given that
bacteria carbon recycling (a key component, see below) is generally preceded by extracellular hydrolysis (e.g. Boetius and Lochte, 1996), the relatively slow and limited respiration
at the deep-sea Atlantic site may reflect a longer bacterial enzyme induction period
assuming that the added carbon was most alien to deep-sea sediments. Under warm bottom
water, the longest delay was encountered at the deepest site (3859 m); respiration peaked
after 12 hours in contrast to 3– 6 hours at the other stations (Fig. 2). Clearly, more
observations, at different time scale, are required.
In our study, we show that respiration, strongly temperature regulated, accounted for a
major part of the benthic response to fresh OM entering the sediments. However, rapid
respiration of algal tracer carbon followed through SCOC is not always evident in deep-sea
sediments. For instance, Blair et al. (1996), Moodley et al. (2002) and Witte et al. (2003a)
did not find significant (within 1–1.5 days) rapid changes in SCOC after adding tracer algal
carbon in cold deep-sea sediments. We believe that this is due to the combination of (1) the
amount of carbon added which may be too low compared to background mineralization
rates, and (2) spatial heterogeneity may obscure detection of changes in SCOC (Witte et
al., 2003a). However, at an Atlantic abyssal site (⬃2°C bottom water temperature,
Witbaard et al., 2000), Witte et al. (2003b) recorded an immediate (within 2.5 days)
significant doubling of SCOC following the addition of fresh algal carbon. Although not
discussed as such, the authors may have provided direct experimental evidence for why
significant changes in SCOC in cold deep-sea sediments are often undetectable (Smith and
Kaufmann, 1999); their addition of fresh algal carbon in amounts equivalent to the annual
input (83 mmol C m⫺2) enhanced SCOC by a mere ⬃0.4 mmol O2 m⫺2 day⫺1. Therefore,
SCOC changes following natural smaller carbon loads of certainly lower reactivity may
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Moodley et al.: Benthic rapid response to phytodetritus deposition
465
indeed be very difficult to detect. In contrast to the measurement of SCOC, 13C-enrichment
in ⌺CO2 is a very sensitive tool to detect respiration of the pre-labeled added carbon. Those
studies that performed this measurement indeed confirm immediate benthic respiration of
fresh OM (Blair et al., 1996; Moodley et al., 2002; this study). The apparent strong
temperature control may also explain why significant temporal changes in SCOC are
readily detected in warm (⬎12°C) Mediterranean deep-sea sediments compared to cold
Atlantic and Pacific deep-sea sediments (see review by Gooday, 2002). However, it should
be noted that the responses recorded in diatom tracer studies may represent a “maximum”
response; the utilized freeze dried diatoms may be a highly degradable carbon source not
directly mimicking in situ input of pre-processed, particulate carbon but clearly demonstrates that benthic respiration of OM matter can be rapid both in shallow and deep-sea
sediments.
Rapid carbon respiration (within 3 to 6 hours, Fig. 2), also in sediment cores almost
devoid of fauna highlights the key role of bacteria, the most ubiquitous benthic component
with evidently sufficient biomass or catabolic capacity even in relatively impoverished
deep-sea sediments. This is supported by direct evidence of bacterial 13C assimilation
(0.2–1.0 mmol C m⫺2, Fig. 1b). Although bacterial 13C incorporation is subject to uncertainties due to conversion factors of PLFA, it clearly demonstrates bacteria assimilation of
the added carbon. Similarly, although it cannot be excluded that the recorded respiration
included that of microbes in the water at the sediment-water interface (the tracer OM was
introduced directly onto the surface of the sediment), we believe the measured response
primarily reflect a benthic response as the sediment-water interface may be considered part
of the benthic environment, and 13C-enrichment in sediment bacteria is direct evidence of a
“true” benthic response. Our findings are in strong contrast with a deep-sea site in the
Atlantic (4800 m water depth, Witte et al., 2003b) where there was no evidence of bacterial
enzyme activity or carbon assimilation within 2.5 days. This may be related to the
difference in the carbon source used in combination with extremely low temperature (2°C);
or as suggested by the authors, bacteria may have been initially out-competed by the fauna,
or carbon became available only after it had passed through the fauna.
Although evidently having limited control on the short-term benthic response to an input
of the utilized fresh OM in terms of respiration (Fig. 1), the effect of community structure
was clearly evidenced in the total amount of added carbon processed and stored in biota as
opposed to unprocessed phytodetritus in the sediment (Fig. 3). While total respiration does
not show a relation with faunal biomass (r 2 ⫽ 0.04), total processing of added label is
significantly correlated with faunal biomass (r 2 ⫽ 0.93). Moreover, only 5% of the added
label enters biota, mainly in bacteria, at sites with low fauna biomass, whereas up to 30% of
the added 13C was recovered in biota at sites supporting a relatively larger biomass
standing stock (Fig. 3). Thus when present, fauna are rapid consumers of fresh phytodetritus (Blair et al., 1996; Levin et al., 1997, 1999; Moodley et al., 2002; Witte et al., 2003a,b;
this study) thereby increasing the amount of added carbon processed. This relationship
between fauna biomass and carbon uptake is also evident when comparing fauna uptake
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Journal of Marine Research
[63, 2
Figure 3. Relationship between fauna and 24 hrs carbon processing in the cross system comparison
(average values at stations 1– 6); on the left y-axis (circles), the impact of fauna on the fraction
biotic assimilation to total carbon processing (respiration ⫹ uptake) and on the second y-axis the
impact of fauna on total processing (squares) and respiration (triangles).
reported for two cold deep-sea sites (1265 m and 4800 m water depth, Witte et al.,
2003a,b), that were offered identical carbon and loading. Similarly, Middelburg et al.
(2000) reported a close relationship between heterotrophic biomass and heterotrophic
short-term uptake of microphytobenthos.
Although fauna may contribute little to immediate respiration of phytodetritus, they
ultimately contribute to respiration either directly through catabolism or indirectly upon
death and decomposition. Fauna assimilation contributes significantly to carbon processing
in fauna rich sediments (Fig. 3) and animals may therefore be an important temporary sink
of labile organic matter in such environments. Moreover, by repackaging OM in their
tissues they directly extend carbon flow pathways and provide a link toward higher trophic
levels. In addition to this direct impact on OM recycling, fauna also indirectly influences
OM remineralization efficiencies in sediments. Fauna mixing or burial of OM, although
increasing carbon availability for biota within the sediment, may slow down overall
respiration of fresh phytodetritus (e.g. van de Bund et al., 2001; Josefson et al., 2002).
However, animal activity (bioturbation and bioirrigation) may enhance remineralization
rates of more refractory OM (e.g. Aller and Aller, 1998). Therefore, depending on the
reactivity of the OM, fauna may strongly affect the time scale of carbon remineralization. It
is common that algal material consists of a more rapidly degradable fraction and slowly
degradable fraction (Westrich and Berner, 1984) and the carbon pool rapidly respired
within 1 day probably represents the most reactive fraction of the added algal OM.
Therefore, with respect to the fate of the remaining, larger fraction of the added carbon,
long-term (manipulative) experiments are required to establish how different components
of fauna versus bacteria affect the fate and OM remineralization capacity of marine
sediments. Not only is this knowledge required to evaluate and better incorporate the
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Moodley et al.: Benthic rapid response to phytodetritus deposition
467
processing agents or biota in models of sediment organic matter decomposition (Smith et
al., 1992; Aller et al., 2001; Mayer et al., 2001) but this also directly relates to a pressing
issue in current marine ecology, the relationship between biodiversity and ecosystem
functioning (e.g. Biles et al., 2002; Bolam et al., 2002).
Acknowledgments. Technical assistance by Ko Verschuure, Pieter van Rijswijk, Joop Nieuwenhuize and Ute Wollenzien is greatly appreciated. The captains and crews of the RV Pelagia, RV
Logachev, and RV Luctor are thanked for their pleasant and professional services. This research was
supported by the Netherlands Organization for Scientific Research, Earth- and Life Sciences
(NWO-ALW). The editor and anonymous reviewers provided helpful comments on this manuscript.
This is publication number 3538 of the NIOO-KNAW, Netherlands Institute of Ecology.
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Received: 1 August, 2004; revised: 2 December, 2004.