Introduction
The burial of organic carbon in marine sediments is a key flux in the global
carbon (C) cycle, linking the surface reactive C reservoirs to long-term
storage in the geological loop. In addition, organic detritus is the main
food source for most benthic ecosystems, and its supply and cycling are thus
important controlling factors for benthic ecology. Furthermore, the
degradation of organic carbon (OC) in sediments usually drives their redox
state, and together these determine nutrient regeneration rates and resupply
to the water column. Estuarine sediments are particularly important locations
for these functions. Of all marine benthic environments, estuarine
(particularly fjordic) and shelf sediments host the largest proportion of
marine sediment C burial (Berner, 1982; Duarte et al., 2005, Smith et al.,
2015). The shallow water depths in estuaries result in the potential of
benthic C burial and nutrient regeneration to control water column
biogeochemistry and productivity (e.g. Middelburg and Levin, 2009).
Therefore, there is a need to understand OC cycling and burial in marine
sediments, and in estuarine sediments in particular.
Previous work has established that factors such as OC loading and degradation
state, sediment grain size, and the time for which OC is exposed to oxygen
before being buried below the oxycline combine to control the relative
importance of remineralisation and burial as a fate of C in marine sediments
(Canfield et al., 1994; Mayer, 1994; Hedges and Keil, 1995; Hartnett et al.,
1998). However, the pathways along which OC may travel towards burial or
remineralisation must be elucidated in order to further our understanding of
benthic C cycling and burial.
There are many processes to which OM arriving at the sediment surface, either
of terrestrial origin delivered through riverine inputs or from surface
phytoplankton production, may be subjected. First, a major fraction of fresh
OC inputs may be fed upon by benthic fauna (Herman et al., 1999; Kristensen,
2001). Thus, C may be assimilated into faunal biomass, and may be transferred
through benthic and/or pelagic food webs. Alternately, ingested sedimentary
OC may survive gut transit and be egested back into the sediment, in which
case it is likely to have been biochemically altered and physically
re-packaged (e.g. Bradshaw et al., 1990a, b, 1991a, b; Woulds et al., 2012,
2014). In addition, at any trophic level of the food web, C may be
metabolised and returned to the water column as CO2. Further, during
bioturbation many fauna transport OC through the sediment column, which may
subject it to fluctuating redox conditions and accelerate decay, or sequester
it at depth below the digenetically active zone (Aller, 1994; Sun et al.,
2002). Secondly, deposited OC will be subject to microbial decay, and may
thus be incorporated into microbial biomass, which itself may then progress
through the food web, or may be returned to the water column as CO2
through microbial respiration. In addition, it may be released as dissolved
organic C (DOC) and re-incorporated into microbial and, subsequently, faunal
biomass through the microbial loop (Pozzato et al., 2013, and references
therein).
As the processes described above are all biologically driven, we will refer
to them collectively as biological C processing (as opposed to long-term C
burial). The relative importance of the different processes, in turn, will be
referred to as the biological C processing pattern.
Isotope tracer experiments with organic matter labelled with an enriched
level of a naturally uncommon stable isotope (typically 13C and/or
15N) are an excellent tool to derive direct quantitative data on
biological C processing patterns and rates (Middelburg, 2014). Such
experiments have been conducted in a wide range of benthic environments, from
estuarine sites (Moodley et al., 2000) to the deep abyssal plain (Witte et
al., 2003b), from OC rich sediments (Woulds et al., 2007) to oligotrophic
sites (Buhring et al., 2006b), and from polar regions (Gontikaki et al.,
2011a, b, c) to the tropics (Aspetsberger et al., 2007; Sweetman et al., 2010).
Many isotope tracer studies have found remineralisation by the entire benthic
community (i.e. bacteria fauna, meiofauna, and macrofauna combined) to form
the dominant fate of the OC supplied (e.g. Woulds et al., 2009; Gontikaki et
al., 2011b). It is reasonably well established that such benthic respiration
rates are strongly controlled by temperature (Moodley et al., 2005) and also
respond to OC input (Witte et al., 2003b) and benthic community biomass (e.g.
Sweetman et al., 2010).
However, considerable variations in carbon processing patterns and rates have
been found between sites, with considerable differences in, for example, the
biomass pools into which OC is dominantly routed. Thus, some studies have
shown that OC uptake by foraminifera and/or bacteria can dominate in both the
short and long term (Moodley et al., 2002; Nomaki et al., 2005; Aspetsberger
et al., 2007), and others have shown a more prominent role for macrofauna
(Witte et al., 2003a). In some cases macrofaunal uptake can even be equal to
total respiration (Woulds et al., 2009). Trends in faunal OC uptake are
usually strongly determined by trends in the biomass of different faunal
groups (e.g. Woulds et al., 2007; Hunter et al., 2012), although this is not
always the case. For example, in sandy subtidal sediments, Evrard et
al. (2010) found that more microphytobenthos C was consumed by meiofauna than
by macrofauna, despite the lower biomass of the former. In cohesive sediments
from a deep fjord, however, the opposite pattern was observed, when
macrofaunal foraminifera ingested less OC than expected based on their
importance in terms of biomass (Sweetman et al., 2009). This was thought to
be due to their relatively deep dwelling lifestyle, suggesting they were not
adapted for rapid feeding on freshly deposited OM. Thus, the ecology and
community structure of any site is thought to exert significant control on
its biological C processing pathways and rates. Furthermore, the examples
given above illustrate how the extreme variability in the abundance and
characteristics of organisms found at seafloor sites throughout the marine
environment has resulted in the lack of a general understanding of how
benthic communities impact seafloor C-cycling patterns and rates.
In a review of isotope tracer experiments carried out in marine sediments,
Woulds et al. (2009) proposed a categorisation of biological C processing
patterns into three main types. “Respiration dominated” sites were defined
as systems in which > 75 % of biologically processed C was
found as respired CO2, and this tended to occur mostly in deep, cold, OM
poor sites with relatively low faunal biomass. “Active faunal uptake”
systems were described as sites in which respiration was still the major fate
of biologically processed C, but where faunal uptake accounted for
10–25 %. This pattern was found in shallower, more nearshore and
estuarine sites, which were richer in OM, and which hosted correspondingly
higher benthic faunal biomass. A third category labelled “metazoan
macrofaunal dominated” displayed an unusual pattern in which uptake by
metazoan macrofauna accounted for > 50 % of biological C
processing, and was chiefly exhibited in a lower oxygen minimum zone site on
the Pakistan margin, where high OC concentrations and just sufficient oxygen
supported an unusually high macrofaunal biomass (an “edge effect”, Mullins,
1985). This categorisation allowed predictions to be made regarding C
processing patterns at a range of sites, but this ability was limited to the
types of benthic environment in which isotope-tracing experiments had been
conducted to that date.
The previously proposed categorisation was limited in the types of benthic
environments covered, and was biased towards subtidal and deep-sea settings
characterised by cohesive sediments. Therefore, a particular environment
missing in previous syntheses was coarse-grained, permeable sediments, such
as are typically found in coastal and shelf environments. One study in
subtidal sandy sediments of the German Bight found unexpectedly rapid C
processing rates, and suggested a C processing pattern that was dominated by
bacterial uptake (Buhring et al., 2006a). However, variation in results
between different experiment durations implies that it could not be used to
propose an additional category. The result was however consistent with
findings that coarse-grained, permeable sediments are capable of more dynamic
biogeochemical cycling than was previously assumed from their generally low
OC contents (Huettel et al., 2014). The rapid biogeochemical cycling is
driven by water flow over roughness on the sediment surface creating local
pressure gradients, which lead to advective exchange of porewaters. This
introduces fresh organic substrates and electron acceptors into the sediment,
and removes metabolites, enhancing OC turnover (Huettel et al., 2014, and
references therein). Therefore, further investigation of biological C
processing in previously understudied permeable sediments is warranted.
Our study aimed broadly to investigate biological C processing rates and
patterns in estuarine sediments. In particular, we aimed to compare
biological C processing in cohesive, fine-grained sediments with that in
permeable, coarse-grained sediments and to contrast the roles played by two
communities with different compositions and structures. We hypothesised that,
in keeping with previous subtidal/shelf/fjordic sites, the cohesive sediments
would exhibit a C processing pattern dominated by respiration but with a
marked role for faunal uptake, while permeable sediments would exhibit rapid
OC turnover and an OC processing pattern dominated by bacterial uptake.
Further, we hypothesised that while faunal C uptake at the two sites would
necessarily involve different taxa, the overall contribution of fauna to
biological C processing would be related to their total biomass.
Methods
Study sites
Two sites were selected for study: one fine-grained, organic carbon-rich
site in Loch Etive and a sandy site with low organic carbon content in the
Ythan estuary.
Loch Etive lies on the west coast of Scotland (Fig. 1). It is a glacier
carved feature, 30 km long, and is divided into three basins by two shallow
sills at Bonawe and Connel. The loch exhibits positive estuarine circulation,
with a strong outflow of freshwater in the surface 10 m, and tidal exchange
of seawater beneath (tidal range is 2 m, Wood et al., 1973). Phytoplankton
standing stock has been found to be relatively high (Wood et al., 1973).
This, combined with input of substantial amounts of terrestrial OC and the
tendency of fine sediment to be resuspended from the shallower areas and
redeposited in the deeper areas (Ansell, 1974), leads to relatively OC rich
sediments in the deep basins. The site chosen for this study lies at the
deepest point (Airds Bay, 70 m) of the middle basin of Loch Etive (Fig. 1).
While the bottom water here is regularly renewed and is therefore well
oxygenated, the sediment has a relatively high oxygen demand, and sulfate
reduction occurs within 5 cm of the sediment–water interface (Overnell et
al., 1996). The experiment was conducted during July 2004, at which point the
bottom water dissolved oxygen saturation was close to 100 %. The sediment
had a median grain size of 21 m with 78 % fines (< 63 m) and
contained ∼ 4.9 wt % organic C (Loh et al., 2008). The benthic
community was dominated by ophuroids, with polychaetes and molluscs also
being abundant (Gage, 1972, C. Whitcraft, unpublished data).
Map showing site locations.
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The Ythan estuary is a well-mixed estuary on the east coast of Scotland
(Fig. 1), 20 km north of Aberdeen. It is ∼ 8 km long, with a mean
width of 300 m. The Ythan sand flat study site was located around halfway
along the estuary on an intertidal sand bar, and exhibited sandy, permeable
and OC poor (∼ 0.1 wt % organic C) sediments (Zetsche et al.,
2011b) which were subject to semi-diurnal tides and seasonal storms. The
median grain size was 336 µm with 11 % fines
(< 63 µm, varying through the year), and the sand is
described as well sorted (Zetsche et al., 2011a). The study site was exposed
at low tide, and covered by 1–2 m of water at high tide. The benthic
community was dominated by oligochaetes, with polychaetes, molluscs,
nematodes and crustaceans also present (Zetsche et al., 2012). The Ythan sand
flat experiment was conducted during May 2008.
Isotope tracing experiments
The experimental set-up varied slightly between sites, to account for the
differences in their depth and sediment grain size.
Loch Etive
Four replicate sediment cores (up to 50 cm depth, 10 cm i.d.) were
collected and placed in a controlled temperature laboratory set to the
ambient temperature of 11 ∘C. Phytodetritus (Thalassiosira,
a representative pelagic species) labelled with 13C (∼ 25 %)
was added to the sediment surface of intact cores to give a dose of
1050 ± 25 mg C m-2 (the standard deviation stated is due to
variation between replicate cores). The cores were then sealed with water
columns of 14–16.5 cm and incubated in the dark for 7 days (156 h). During
the incubation, the oxygen concentration in core-top water was maintained by
pumping the water through an “oxystat” gill, composed of gas permeable
tubing submerged in a reservoir of 100 % oxygenated seawater (see Woulds
et al., 2007) and monitored with Clark-type electrodes. As the tubing used in
the oxystat gill was permeable to all gases, there was the potential for loss
of some 13CO2 generated during the experiment. However, the
dissolved inorganic carbon (DIC) concentration difference between the
incubation water and oxygenated reservoir will have remained small; thus,
this effect is thought to be minor. Samples of the overlying water were taken
at 0, 24, 48, 72, 96, 120 and 144 h after the introduction of the labelled
phytodetritus. These were preserved in glass vials without a headspace and
poisoned with HgCl2 for DIC and δ13C-DIC analysis.
At the end of the incubation period, cores were sectioned at intervals of
0.5 cm up to 2 cm depth, then in 1 cm sections up to 10 cm depth, and
finally in 2 cm sections up to 20 cm depth. Half of each sediment slice was
sieved, with > 300 µm (macrofauna) and
150–300 µm (meiofauna) fractions retained. The other half of each
slice was stored frozen in plastic bags. Sieve residues were examined under
the microscope and all fauna were extracted. Organisms were sorted to the
lowest taxonomic level possible and preserved frozen in pre-weighed tin boats
and pre-combusted glass vials. Fauna from two of the four cores were allowed
to void their guts before preservation. This was achieved by allowing them to
remain in dishes of filtered seawater for several hours before freezing.
The Ythan sand flat
Four replicate sediment cores were collected by pushing 25 cm diameter
acrylic core tubes into the sediment at low tide, and digging them out to
obtain intact sediment cores 14–15 cm in length. These were returned to a
controlled temperature laboratory set to 11 ∘C at Oceanlab,
University of Aberdeen. Filtered Ythan estuary water was added to each core
to create a water column. A lid was placed on each core, leaving a headspace,
with exhaust ports open. Fully oxygenated conditions were maintained by
gentle bubbling with air, except during respiration measurements (see below).
Lids were mounted with stirring disks, the rotation rates of which were
calibrated to generate appropriate pressure gradients to prompt porewater
advection (Erenhauss and Huettel, 2004). The overlying water was changed
daily. Isotopically labelled (34 % 13C) phytodetritus (freeze-dried
Navicula incerta, a representative benthic species) was added to the
water column and allowed to sink onto the sediment–water interface to give a
dose of 753 ± 9.4 mg C m-2. Twice during the subsequent 7 days
(immediately after phytodetritus addition and 5 days later) the respiration
rate in each core was measured. This involved filling the headspace in each
core to exclude all air bubbles and sealing all lids. Time series water
samples were taken over the subsequent 24 h and preserved for
δ13C-DIC analysis as described above. At the end of each
respiration measurement, lids were removed and dissolved oxygen was measured
by Winkler titration to ensure it had not declined by more than 20 %.
The experiment lasted 7 days (162 h), after which the overlying water was
removed and a 5 cm diameter sub-core was taken from each core. This was
sectioned at 1 cm intervals and frozen. The remaining sediment was sectioned
at intervals of 0–1, 1–2, 2–3 and 3–5 cm, and sieved on a
500 µm mesh. Sediment and fauna remaining on the sieve were
preserved in buffered 10 % formaldehyde in seawater. Fauna were picked
from sieve residues under a microscope, identified, and placed in glass vials
or pre-weighed silver capsules.
Analysis
Bulk stable isotope analyses
Fauna samples were oven-dried at 45∘C. Fauna with calcite skeletons
(ophiuroids, molluscs, and foraminifera) were de-carbonated by the addition
of a few drops of 6 N HCl. For soft-bodied fauna, 1 N HCl was used to
eliminate possible traces of carbonates. In all cases whole organisms were
analysed. In the Loch Etive experiment fauna from two replicate cores were
allowed time to void their guts, but it was not clear that they actually did
so (see below). All samples were dried at ∼ 50∘C before
analysis for OC content and δ13C.
Loch Etive samples were analysed on a Europa Scientific (Crew, UK) Tracermass
isotope ratio mass spectrometer (IRMS) with a Roboprep Dumas combustion
sample converter. Appropriately sized samples of acetanilide were used for
quantification, and all C abundance data were blank corrected. Replicate
analyses revealed relative standard deviations of 4.6 % for C abundance
and 0.7 ‰ for δ13C. Ythan sand flat samples were analysed
using a Flash EA 1112 Series Elemental Analyser connected via a Conflo III to
a DeltaPlus XP isotope ratio mass spectrometer (all ThermoFinnigan,
Bremen, Germany). Carbon contents of the samples were calculated from the
area output of the mass spectrometer calibrated against National Institute of
Standards and Technology standard reference material 1547 (peach leaves),
which was analysed with every batch of ten samples. The isotope ratios were
traceable to International Atomic Energy Agency reference materials USGS40
and USGS41 (both L-glutamic acid), certified for δ13C (‰).
Long-term precisions for a quality control standard (milled flour) were total
carbon 40.3 ± 0.35 % and δ13C
-25.4 ± 0.13 ‰.
Overlying water samples were analysed for concentration and δ13C
of DIC as described by Moodley et al. (2000). Briefly, a He headspace was
created in sample vials, the CO2 and δ13C of which were
quantified using a Carlo Erba MEGA 540 gas chromatograph and a Finnigan Delta
S isotope ratio mass spectrometer, respectively. The system was calibrated
with acetanilide (Schimmelmann et al., 2009) and the IAEA-CH-6 standard.
Repeat analyses of standard materials gave a relative standard deviation of
4.4 % for DIC concentrations and a standard deviation of
±0.09 ‰ for δ13C.
Bacterial phospholipid fatty acids (PLFAs)
Aliquots of sediment were treated with a Bligh and Dyer extraction, involving
shaking at room temperature in a 2:1:1 mix of methanol, chloroform, and
water. Lipids were recovered in the chloroform layer and were loaded onto
silica gel columns. Polar lipids were eluted in methanol and methylated in
the presence of methanolic NaOH. The C12:0 and C19:0 fatty acid methyl esters
were used as internal standards. Fatty acids were separated by gas
chromatography on a 30 m, 0.25 mm i.d., 25 µm film thickness
BPX70 column and combusted in a Thermo GC-combustion II interface. Isotope
ratios were then determined using a Thermo Delta+ isotope ratio mass
spectrometer (for further details, see Woulds et al., 2014).
Data treatment
Uptake of added C by fauna is reported in absolute terms (see below), and as
isotopic enrichments over the natural background faunal isotopic composition.
Isotopic compositions were expressed as δ13C, derived using
Eq. (1).
δ‰=RsRr-1×1000,
where Rs and Rr are the 13C / 12C ratio
in the sample and the reference standard, respectively. Isotopic enrichments
(Δδ) were then calculated using Eq. (2).
Δδ=δ13Csample-δ13Cbackground
Carbon uptake by faunal groups was calculated by subtracting naturally
occurring 13C, multiplying by the sample C contents, and correcting for
the fact that the added phytodetritus was not 100 % 13C labelled, as
shown in Eq. (3):
C Uptakesample (µg)=at%sample-at%background×C
Contentssampleat%phytodetritus×100,
where at % is the 13C atoms present as a percentage of the total C
atoms present. Data from individual specimens were summed to produce faunal C
uptake by different groups of fauna. For Loch Etive, background 13C was
subtracted based on natural faunal isotopic data collected concurrently with
the C tracing experiment. For the Ythan sand flat, natural faunal isotopic
data were not available, and instead the natural C isotopic signature of
sedimentary organic C (-20.2 ‰) was used. Isotopic signatures of
fauna at the end of the experiment had a maximum of 2460 ‰ and a
mean of 175 ‰. Therefore the small inaccuracies introduced by the
use of this natural background value will not have been significant.
The DIC concentrations and δ13C-DIC were used to calculate the
total amount of added 13C present as DIC in experimental chambers at
each sampling time. A linear regression was applied to these to yield a
separate respiration rate for each core and for each period of respiration
measurement (mean R2=0.909, with the exception of one measurement
showing poor linearity with R2=0.368), and the rate was multiplied by
experiment duration to calculate total respiration of added C during the
experiment. In the case of the Ythan sand flat respiration was measured
during two separate 24 h periods through the experiment. In this case
average rates from the two measurements were used to calculate total
respiration of added C throughout the experiment.
Bacterial C uptake was quantified using the compounds iC14:0, iC15:0,
aiC15:0, and iC16:0 as bacterial markers. Bacterial uptake of added C was
calculated from their concentrations and isotopic compositions (corrected for
natural 13C occurrence using data from unlabelled sediment), based on
these compounds representing 14 % of total bacterial PLFAs, and bacterial
PLFA comprising 5.6 % of total bacterial biomass (Boschker and
Middelburg, 2002). In the case of Loch Etive, the sediments from which PLFAs
were extracted had previously been centrifuged (10 min, 3500 rpm, room
temperature) for porewater extraction, which could have led to a slight
reduction in the bacterial biomass and C uptake measured.
Results
The mean recovery of added C from the bacterial, faunal and respired pools
together was 30 ± 6 and 31 ± 10 % of that which was added for
Loch Etive and the Ythan sand flat, respectively. This is a good recovery
rate compared to other similar experiments (e.g. Woulds et al., 2007). Most
of the remaining C was likely left in the sediment as particulate organic C
or as dissolved organic C.
Remineralisation
The average respiration rate of the added OC was similar in Loch Etive and on
the Ythan sand flat, and reached 0.64 ± 0.4 and
0.63 ± 0.12 mg C m-2 h-1, respectively. Thus, the total
amount of added C that was respired at each site (over 156 h in Loch Etive
and 162 h on the Ythan sand flat) was 99.5 ± 6.5 and
102.6 ± 19.4 mg C m-2 for Loch Etive and the Ythan sand flat,
respectively (Fig. 2). In both experiments, respiration rates measured in the
first 48 h (1.41 ± 0.14 and
0.74 ± 0.02 mg C m-2 h-1 for Etive and the Ythan sand
flat, respectively) were higher than those measured in the last 48 h of the
experiment (0.31 ± 0.04 and 0.52 ± 0.22 mg C m-2 h-1
for Etive and the Ythan sand flat, respectively; this difference was
significant only for Loch Etive, t test, P< 0.001). The increase
in labelled DIC over time for each chamber is shown in Fig. S1 in Supplement.
The distribution of initially added C between different biological
pools at the end of the experiments in absolute terms (upper panel), and as
percentages of total biological C processing (lower panel). Note there are no
data for meiofaunal or foraminiferal uptake on the Ythan sand flat.
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Faunal biomass and C uptake
Macrofaunal biomass in the experimental cores was
4337 ± 1202 mg C m-2 in Loch Etive and
455 ± 167 mg C m-2 on the Ythan sand flat. Macrofaunal
δ13C signatures (for individual specimens) reached maximal values
of 7647 and 2460 ‰ in Loch Etive and on the Ythan sand flat,
respectively. Total faunal C uptake was orders of magnitude greater in Loch
Etive (204 ± 72 mg C m-2) than on the Ythan sand flat
(0.96 ± 0.3 mg C m-2) (Fig. 2). This difference was driven
partly by a difference in biomass, but fauna on the Ythan sand flat were also
comparatively less active, as reflected by biomass-specific C uptake at the
two sites (0.047 ± 0.01 and 0.0022 ± 0.0006 mg C uptake per mg C
biomass for Loch Etive and the Ythan sand flat, respectively).
In Loch Etive, both faunal biomass and carbon uptake were dominated by two
ophuroids, Amphiura fillaformis and A. chiajei, which
contributed 75 and 95 % to the total biomass and to faunal C uptake,
respectively (Fig. 3). The molluscs and polychaetes contributed 11 and
6 % to biomass, but only 1.6 and 1 % to faunal C uptake,
respectively. Amongst the polychaetes, the Flabelligeridae and
Harmothoe tended to show lower 13C enrichment (i.e. a lower
specific uptake of labelled C), while representatives of all other families
(Capitellidae, Syllidae, Cirratulidae,
Cossura, and Terebellidae) showed much higher levels of
labelling.
Taxa responsible for biomass and C uptake in (a) Loch Etive
and (b) the Ythan sand flat.
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On the Ythan sand flat, the macrofaunal community was dominated by
oligochaetes and nematodes (Fig. 3). The proportion of total faunal C uptake
accounted for by oligochaetes (48 %) approximately matched their
contribution to faunal biomass (51 %). However, nematodes contributed
slightly less towards total faunal uptake (14 %) than they did to total
biomass (19 %). Other minor groups included amphipods (0.3 % of
biomass), polychaetes (2 % of biomass) and gastropods (1.5 % of
biomass). Of these groups, the polychaetes and gastropods made
disproportionately large contributions to faunal C uptake, accounting for
10 % and 18 %, respectively (Fig. 3).
In the Loch Etive experiment, metazoan meiofaunal and foraminiferal data were
also collected. Metazoan meiofaunal and foraminiferal biomasses in
experimental cores were 47 ± 14 mg C m-2 and
343 ± 625 mg C m-2, respectively. These two groups showed
maximal Δδ13C values of 1360 and 3313 ‰,
respectively. Metazoan meiofauna were not taxonomically sorted, but amongst
the foraminifera the highest labelling was observed in Crithionina
sp., while Pelosina did not show measurable label uptake. Compared
to the macrofauna, meiofaunal C uptake was minor, at 0.18 ± 0.20 and
5.21 ± 5.15 mg C m-2 for metazoans and foraminifera,
respectively (Fig. 2). Thus, metazoan meiofauna and foraminifera contributed
1 and 7 % to the total faunal biomass, and 0.1 and 2.5 % to faunal C
uptake, respectively.
Bacterial biomass and C uptake
Bacterial biomass in the surface 5 cm of sediment in Loch Etive was
5515 ± 3121 mg C m-2, and on the Ythan sand flat it was
7657 ± 3315 mg C m-2. The amount of added C incorporated into
bacterial biomass was 2 orders of magnitude greater on the Ythan sand flat
(127 ± 89 mg C m-2) than in Loch Etive
(1.80 ± 1.66 mg C m-2, Fig. 2). In the majority of cores,
> 90 % of bacterial uptake occurred in the top 3 cm of
sediment. However, in one core from Loch Etive, 28 % of bacterial uptake
occurred between 3 and 6 cm depth. In comparison, 52 % of the bacterial
biomass from the top 5 cm occurred shallower than 3 cm for Loch Etive, and
this value was 66 % on the Ythan sand flat. Biomass-specific uptake for
the bacteria was 2 orders of magnitude greater on the Ythan sand flat
(0.016 ± 0.004 mg C uptake per mg C biomass) than in Loch Etive
(0.00023 ± .00013 mg C uptake per mg C biomass). Thus it appears that
the rapid uptake of added C by bacteria at the sandy site was primarily
driven by a more active bacterial community, rather than by a larger
bacterial biomass.
Biological carbon processing patterns
The large differences in macrofaunal and bacterial C uptake rates between the
two sites resulted in markedly different biological C processing patterns
(Fig. 2). In both cases, respiration was an important, but usually not the
dominant, fate of biologically processed C, accounting for 25–60 %. In
the case of Loch Etive, the dominant fate of biologically processed C was
macrofaunal uptake (64 ± 10 %), and this also resulted in a greater
amount of total biological C processing (Fig. 2) than on the Ythan sand flat.
On the Ythan sand flat, bacterial uptake (48 ± 18 %) was the
dominant fate of biologically processed C. In Loch Etive, uptake of C by
bacterial, metazoan meiofaunal, and foraminiferal communities made only minor
contributions to total biological C processing (Fig. 2). On the Ythan sand
flat, macrofaunal uptake made a relatively minor contribution (Fig. 2).
Unfortunately, uptake by meiofaunal organisms could not be quantified at the
latter site.
Discussion
Experimental approach
This study compares data from two experiments which, while following the same
principle, nevertheless had slightly different experimental set-ups. The
water depth, core size, stirring regime, light availability and C dose added
all differed between the two study sites. The differences in stirring regime
and light availability were enforced to properly replicate natural conditions
in each experiment; thus, any contrasts caused by these conditions reflect
differences in functioning of the two habitats. The presence of light in the
Ythan sand flat experiment means it is possible that some labelled DIC
produced by respiration may have been utilised during photosynthesis, leading
to an underestimation of respiration rate. However, as the isotopic labelling
level of DIC always remained below 1.33 at %, this is unlikely to have
had a measurable effect. The difference in water depth and core diameters was
driven by the practicality of collecting undisturbed sediment cores from the
two contrasting sediment types. While the difference in depth means that
photosynthesis and flux of CO2 gas to the atmosphere during emergent
periods would normally occur on the Ythan sand flat but not in Loch Etive,
they remain comparable in their temperatures and estuarine locations. The
difference in C dose added was minor (∼ 25 %) and also driven by
practical constraints. Previous studies have found little impact of such
minor differences in C dose (Woulds et al., 2009). Where the amount of added
C has been observed to control biological processing patterns and rates, the
difference in C dose has been much more pronounced (10-fold, Buhring et al.,
2006b). We acknowledge that the C dose represented a different proportion of
naturally present OC at each site, and this could have led to an enhanced
response at the Ythan sand flat. However, surface sediment OC concentrations
are not necessarily a good reflection of actual C delivery to the seafloor,
given the different transport mechanisms in permeable and cohesive sediments
(see below). Further, there is a sparsity of data available on primary
production rates, particularly for the Ythan sand flat. Therefore maintaining
a uniform C addition was judged to yield the most comparable data. Thus,
while experimental details varied between Loch Etive and the Ythan sand flat,
we are confident that direct comparisons between the results of the two
experiments are valid.
Due to practical constraints, meiofauna were not included in the analysis of
the Ythan sand flat experiment. Previous studies have found both that
meiofauna consume disproportionate amounts of C relative to their biomass
(Evrard et al., 2010) and that nematodes (a major meiofaunal group) made a
negligible contribution to C cycling (Moens et al., 2007). We are unable to
speculate how active the meiofauna were in C cycling in the present study,
but, despite wide variations in the importance of meiofaunal uptake (Nomaki
et al., 2005; Sweetman et al., 2009; Evrard et al., 2010), it is usually
similar to or less than macrofaunal C uptake (Nomaki et al., 2005; Evrard et
al., 2010). Thus, we consider it unlikely that the meiofaunal community was
involved in C processing on the same scale as observed for bacterial uptake
and total respiration, and exclusion of meiofauna in the Ythan sand flat
experiment is unlikely to have markedly altered the overall pattern of
biological C processing that we observed.
There was a difference in the sieve mesh sizes used to collect macrofauna in
the two experiments (300 µm in Loch Etive and 500 µm on
the Ythan sand flat). The use of larger mesh sizes is more conventional and
practical in coarser-grained sediments. The larger mesh used on the Ythan
sand flat is likely to have reduced the macrofaunal biomass and C uptake
measured. However, the effect is likely to have been insufficient to explain
the striking differences in macrofaunal C uptake and biomass-specific uptake
seen between the two sites.
Finally, the majority of fauna were too small for manual removal of gut
contents, and were therefore analysed with their gut contents in place. The
exception to this was two of the Loch Etive cores, which were allowed time to
void their guts before freezing. However, this did not produce a significant
difference in the macrofaunal 13C pool between those cores and the other
two in which fauna retained their gut contents (Mann–Whitney, p=0.245).
Some infauna respond to starvation by retaining their gut contents for days
or weeks. Therefore it is possible that organisms either voided their guts
incompletely, or not at all. It is also possible that the amount of added C
residing in macrofaunal guts was comparatively small, as shown by Herman et
al. (2000), and thus not measurable above variation caused by faunal
patchiness. Thus the values reported here as faunal C uptake include C in
both gut contents' faunal tissue.
Respiration rates
The respiration rates observed in Loch Etive and on the Ythan sand flat were
very similar (Fig. 2). This is unsurprising, as the two experiments were
conducted at the same temperature, and similar C loadings were applied.
Temperature is known to control sediment respiration rates through impacts on
diffusion and microbial process rates (Yvon-Durochet et al., 2015), and
benthic respiration has been shown to respond to temperature changes with a
Q10 of 2–3 (Kristensen, 2000). Further, after manipulating the
temperatures at which cores from both a deep-sea site and an estuarine site
were incubated, Moodley et al. (2005) found similar respiration rates of
added phytodetritus at similar temperatures, despite differences in water
depth and faunal community. Our finding of similar rates of respiration,
despite marked differences in influential factors such as macrofaunal
biomass, organic C concentration, and solute transport processes (Kristensen,
2000; Hubas et al., 2007; Huettel et al., 2014), supports the suggestion that
temperature is the dominant control.
Faunal uptake
In Loch Etive, the macrofauna overwhelmingly dominated total faunal C uptake
(accounting for 97 %) compared to metazoan meiofauna (0.1 %) and
foraminifera (2.5 %). These contributions were broadly similar to their
contributions to total faunal biomass (92, 1 and 7 % for macrofauna,
metazoan meiofauna and foraminifera, respectively). Thus, in line with
previous findings (Middelburg et al., 2000; Woulds et al., 2007; Hunter et
al., 2012), the distribution of C uptake amongst faunal classes was largely
determined by the relative biomass of each group. The dominance of faunal C
uptake by macrofauna has been observed previously. For example, in shorter
experiments on the Porcupine Abyssal Plain (Witte et al., 2003b), in the deep
Sognefjord (Witte et al., 2003a) and at certain sites on the Pakistan margin
(Woulds et al., 2007), macrofauna dominated faunal C uptake, and at an
Antarctic site, Moens et al. (2007) found that meiofaunal nematodes made a
negligible contribution to C uptake. However, uptake into the macrofaunal
pool can be most important during the initial response to an OC pulse, with
bacterial uptake and respiration becoming more important over longer
timescales (Moodley et al., 2002; Witte et al., 2003b). Also in contrast to
the findings above, metazoan meiofaunal and foraminiferal uptake have
previously been shown to be more important pathways for C (e.g. Moodley et
al., 2000). Where macrofauna are absent, or where conditions are
unfavourable, smaller taxa can dominate C uptake, such as within the Arabian
Sea oxygen minimum zone (Woulds et al., 2007). At other sites, meiofauna and
foraminifera have been shown to take up more C than macrofauna without the
presence of a stress factor. This was the case at 2170 m water depth in the
north-east Atlantic, in Sagami Bay and at a subtidal Wadden Sea site;
foraminifera and meiofauna have been observed to consume more C than
macrofauna, sometimes despite having lower biomass (Moodley et al., 2002;
Nomaki et al., 2005; Evrard et al., 2010).
The marked uptake of C by macrofauna in Loch Etive was largely driven by two
species of ophuroid, which also dominated the macrofaunal biomass (Fig. 3).
However, the ophuroids accounted for a greater percentage of macrofaunal C
uptake than they accounted for macrofaunal biomass (Fig. 3), and thus were
disproportionately responsible for macrofaunal C uptake. On the Ythan sand
flat, the contribution to C uptake by the dominant oligochaetes was in line
with their biomass (both ∼ 50 %, Fig. 3). However, other faunal
groups contributed differently to biomass and C uptake. Nematodes were
responsible for less C uptake than expected, while the polychaetes,
amphipods, and molluscs fed comparatively efficiently on the added C. This is
in line with previous studies in which certain polychaete families have been
found to be selective or rapid feeders on fresh algal detritus (e.g. Woulds
et al., 2007).
When C uptake is plotted against biomass for each faunal specimen analysed
across both study sites, a positive correlation is apparent (Fig. 4). This
correlation has been reported previously (Moodley et al., 2005; Woulds et
al., 2007), and suggests that faunal C uptake is largely driven by faunal
biomass, despite the fact that they are auto-correlations (uptake data are
derived by multiplying C contents of a specimen by its isotopic signature).
Within each site the distribution of C uptake amongst faunal groups was also
predominantly driven by biomass. However, the lower faunal biomass on the
Ythan sand flat does not fully explain the lower faunal C uptake observed
there, as biomass-specific C uptake was also considerably lower than in Loch
Etive. We suggest that the low OC standing stock in the permeable sediment of
the Ythan sand flat supports a lower biomass and a less active faunal
community with lower metabolic rates.
Log10 uptake against Log10 C biomass for (a) all
specimens analysed in Loch Etive and on the Ythan sand flat, (b)
Loch Etive with taxonomic detail, and (c) the Ythan sand flat with
taxonomic detail.
![]()
The identity of fauna responsible for C uptake was in line with expectations
from some previous studies, but not with others, and the reasons for this
variation are not clear. Therefore, while overall faunal uptake is dictated
by biomass, it remains challenging to predict which faunal groups and taxa
will dominate C uptake in a particular benthic setting. This appears to be
determined by the complex interplay of factors that determine benthic
community composition, such as the nature and timing of food supply (Witte et
al., 2003a, b), environmental stressors (Woulds et al., 2007), feeding
strategies, and competition (Hunter et al., 2012).
Total biological C processing rates
Loch Etive showed the largest amount of total biologically processed C
(Fig. 2). As both sites showed very similar respiration rates, the difference
in total biological C processing was driven by greater faunal uptake in Loch
Etive (Fig. 2), and this was a result of greater faunal biomass. The
relationship between biomass and total biological C processing is also shown
by data gathered from previously published isotope tracing experiments
(Table 1), which show a correlation between total biomass (faunal plus
bacterial) and total biological C processing rate (Pearson's correlation,
r=0.499, p=0.002). We therefore suggest that benthic community structure
impacts the total C processing capacity of benthic environments, through a
relationship between biomass and total biological C processing rates, with an
emphasis on the importance of macrofaunal biomass as indicated by the
importance of macrofauna in Loch Etive, and the fact that the proportion of
the bacterial biomass which is active can be rather variable (see below).
Short-term biological C processing categories
The distribution of biologically processed C between different C pools
(biological C processing pattern, Fig. 2) varied markedly between the two
sites. While they both showed respiration to be an important process, the
dominant fate of biologically processed C in Loch Etive was uptake by
macrofauna, while on the Ythan sand flat it was uptake by bacteria (Fig. 2).
A review of previous isotope tracing experiments proposed a categorisation of
short-term biological C processing patterns (Woulds et al., 2009), which can
be used as a framework to explain patterns observed in this study.
Loch Etive was expected to show a short-term biological C processing pattern
in line with the category labelled “active faunal uptake”. In this
category, biological C processing is dominated by respiration, but faunal
uptake accounts for 10–25 % (Woulds et al., 2009). This category is
found in estuarine and nearshore sites which are warmer than the deep sea,
have slightly more abundant OM, and thus support higher biomass and more
active faunal communities. However, the short-term biological C processing
pattern observed in Loch Etive was most similar to the category labelled
“macrofaunal uptake dominated” (Fig. 5), in which uptake of C by macrofauna
accounts for a greater proportion of biologically processed C than total
community respiration (Woulds et al., 2009). This is an unusual pattern,
previously only observed in the lower margin of the Arabian Sea oxygen
minimum zone. It was hypothesised in that case that the occurrence of a
macrofaunal population capable of this magnitude of C uptake was due to the
presence of particularly high OC concentrations in the sediment, coupled with
sufficient oxygen for larger organisms. This explanation also applies to Loch
Etive, where the sediment OC concentration was nearly 5 %. In contrast to
the Arabian Sea site however, Loch Etive featured fully oxygenated bottom
water. Thus, the occurrence of macrofaunal uptake dominated short-term
biological C processing appears to be facilitated by high OC availability,
rather than by low oxygen conditions. Experiments conducted in Pearl Harbor
sites impacted by invasive mangroves also show OC availability controlling
the relative importance of faunal C uptake (Sweetman et al., 2010). A control
site was OC poor (0.5 % wt % OC) and showed respiration dominated
biological C processing (Fig. 5), while a nearby site from which invasive
mangroves had been removed showed active (macro)faunal uptake (Fig. 5), in
line with higher sediment OC content (3.1 % wt % OC) and an elevated
macrofaunal biomass.
Biological C processing pattern categories adapted from Woulds et
al. (2009), with the experiments from this study and the new category
“bacterial uptake dominated” added. Data sources are as follows: eastern
Mediterranean (E. Med.), north-eastern Atlantic, northern Aegean (N. Aegean)
and Scheldt Estuary 2: Moodley et al. (2005); Pakistan margin (Pak. 140, 300,
940, and 1850 m): Woulds et al. (2009); Sognefjord: Witte et al. (2003 a);
Scheldt Estuary 1: Moodley et al. (2000); Pearl Harbour: Sweetman et
al. (2010); Gulf of Gdansk: Evrard et al. (2012); German Bight: Buhring et
al. (2006).
![]()
We hypothesised that the Ythan sand flat would show a short-term biological C
processing pattern that did not fit with the categories suggested by Woulds
et al. (2009). Our hypothesis was supported, as biological C processing on
the Ythan sand flat was dominated by bacterial C uptake (Fig. 2). There have
been indications in previous isotope tracing experiments in sandy sediments
of the German Bight that bacterial C uptake may be particularly important in
sandy sediments (Buhring et al., 2006a). Thus we now combine the previous and
current results and propose a new biological C processing category labelled
“bacterial uptake dominated” (Fig. 5). In the new category, bacterial
uptake is the dominant short-term fate of biologically processed C,
accounting for ∼ 35–70 %. Respiration remains important,
accounting for 25–40 % of biologically processed C, and faunal uptake
tends to account for ∼ 5–20 %.
The new category of biological C processing so far has only been observed in
two experiments targeting sandy, permeable sediments, and so the features of
such sediments appear to favour bacterial C uptake. Advective porewater
exchange in permeable sediments has been shown to enhance the rates of
microbial processes such as remineralisation and nitrification (Huettel et
al., 2014) through rapid supply of oxygen and flushing of respiratory
metabolites. This is balanced by introduction of fresh OC as algal cells are
filtered out of advecting porewater (Ehrenhauss and Huettel, 2004); thus,
substrate and electron acceptors for bacterial respiration are supplied.
While permeable sediments generally have similar or lower bacterial
abundances than muddy sediments, their bacterial communities tend to be
highly active, and it has been suggested that, because they are subjected to
rapidly changing biogeochemical conditions, they are poised to respond
rapidly to OC input (Huettel et al., 2014). Notably however, the rapid rates
of bacterial activity observed in permeable sediments do not typically lead
to build-up of bacterial biomass (Huettel et al., 2014). This may be due to
regular removal of bacterial biomass during sediment reworking, in line with
observations of seasonal changes in clogging of pore spaces in sandy
sediment (Zetsche et al., 2011a).
Sources and site details of previous isotope tracing experiment
data. PAP = Porcupine Abyssal Plain. For Woulds et al. (2009)
experiments, PM is the Pakistan margin, “pre” and “post” indicate pre- or
post-monsoon seasons, and 2d or 5d indicate approximate experiment durations
in days. In some other cases experiment durations are indicated in hours
(h).
Source
Site/experiment
Depth
Temperature
Incubation duration
Macrofaunal biomass
Bacterial biomass
Respiration rate
Total processing rate
(m)
(∘C)
(h)
(mg C m-2)
(mg C m-2)
(mg C m-2 h-1)
(mg C m-2 h-1)
Moodley et al. (2000)
Oosterschelde
Intertidal
10
6
n.d.
nd
7.758
13.150
Moodley et al. (2002)
North-western Spain
2170
3.6
35
39
2
0.083
0.290
Witte et al. (2003b)
PAP 60 h
4800
n.d.
60
120
2500
0.167
0.225
Witte et al. (2003b)
PAP 192 h
4800
n.d.
192
120
2500
0.167
0.188
Witte et al. (2003b)
PAP 552 h
4800
n.d.
552
120
2500
0.236
0.263
Witte et al. (2003a)
Sognefjord 36 h
1265
7
36
250
8500
0.539
0.781
Witte et al. (2003a)
Sognefjord 72 h
1265
7
72
250
8500
0.451
0.715
Moodley et al. (2005)
North Sea (perturbed)
37
6
24
756
2688
0.600
0.735
Moodley et al. (2005)
N. Agean
102
14
24
73
522
2.895
3.075
Moodley et al. (2005)
N. Agean
698
14
24
37
366
3.110
3.290
Moodley et al. (2005)
E. Med.
1552
14
24
6
254
2.750
2.830
Moodley et al. (2005)
E. Med.
3859
14
24
4
312
2.495
2.610
Moodley et al. (2005)
North-eastern Atlantic 24 h
2170
4
24
138
313
0.300
0.330
Moodley et al. (2005)
North Sea
37
16
24
732
2304
3.025
3.600
Moodley et al. (2005)
Estuary
Intertidal
18
24
1356
1260
2.545
3.705
Bhuring et al. (2006)
German Bight 12 h
19
9
12
n.d.
nd
0.258
3.592
Bhuring et al. (2006)
German Bight 30 h
19
9
30
n.d.
n.d.
0.620
2.523
Bhuring et al. (2006)
German Bight 132 h
19
9
132
n.d.
n.d.
0.258
0.667
Bhuring et al. (2006)
German Bight in situ
19
13
32
n.d.
n.d.
0.338
2.834
Woulds et al. (2009)
PM pre 140 2 d
140
22
68
110
1100
2.827
3.750
Woulds et al. (2009)
PM post 140 2 d
140
22
44
110
1100
2.066
2.977
Woulds et al. (2009)
PM post 140 5 d
140
22
118
110
1100
1.164
1.611
Woulds et al. (2009)
PM post 140 in situ
140
22
60
110
1100
0.705
0.955
Woulds et al. (2009)
PM pre 300 2 d
300
15
61
0
1000
0.365
0.487
Woulds et al. (2009)
PM pre 300 5 d
300
15
127
0
1000
0.285
0.386
Woulds et al. (2009)
PM post 300 2 d
300
15
58
0
1000
0.527
0.931
Woulds et al. (2009)
PM post 300 5 d
300
15
155
0
1000
0.477
0.865
Woulds et al. (2009)
PM post 300 in situ
300
15
60
0
1000
0.035
0.250
Woulds et al. (2009)
PM pre 850 2 d
850
10
46
nd
nd
1.064
1.934
Woulds et al. (2009)
PM pre 940 5 d
940
9
112
910
700
0.469
0.933
Woulds et al. (2009)
PM post 940 5 d
940
9
113
910
700
0.486
1.274
Woulds et al. (2009)
PM post 940 in situ
940
9
48
910
700
0.155
0.986
Woulds et al. (2009)
PM pre 1000 2 d
1000
8
57
nd
nd
0.990
2.411
Woulds et al. (2009)
PM pre 1200 5 d
1200
7
114
60
nd
0.274
0.289
Woulds et al. (2009)
PM pre 1850 2 d
1850
3
48
110
300
0.065
0.235
Woulds et al. (2009)
PM pre 1850 5 d
1850
3
117
110
300
0.434
0.506
Woulds et al. (2009)
PM post 1850 5 d
1850
3
86
110
300
2.459
2.623
Sweetman et al. (2010)
Pearl Harbour control
Intertidal
24
48
337
5500
3.835
4.343
Sweetman et al. (2010)
Pearl Harbour removal
Intertidal
24
48
3391
4500
5.349
7.401
Sweetman et al. (2010)
Pearl Harbour mangrove
Intertidal
24
48
713
18154
5.456
6.048
Sweetman et al. (2010)
Kaneohe Bay control
Intertidal
24
48
882
3500
6.125
6.849
Sweetman et al. (2010)
Kaneohe Bay removal
Intertidal
24
48
1435
9000
5.295
7.475
Evrard et al. (2010)
Wadden Sea
Photic subtidal
15
96
nd
nd
0.031
0.034
Evrard et al. (2012)
Gulf of Gdansk (sandy)
1.5
20
72
558
407
0.047
0.061
This study
Loch Etive
70
11
156
4337
5515
0.638
1.994
This study
Ythan sand flat
Intertidal
11
162
455
7657
0.633
1.421
The domination of short-term biological C processing by bacterial uptake
implies a high value for bacterial growth efficiency (BGE). This is
calculated as bacterial secondary production divided by the sum of bacterial
secondary production and bacterial respiration. Bacterial respiration is not
quantified here; however, it is likely that a large proportion of total
community respiration is attributable to bacteria (Schwinghamer et al., 1986;
Hubas et al., 2006). For the sake of discussion, BGE has been approximated
for the Ythan sand flat experiments as bacterial C uptake divided by the sum
of bacterial C uptake and total community respiration, giving a conservative
estimate of 0.51 ± 0.18. This is at the high end of the range of values
(< 0.05 to > 0.5) reported in a review of growth
efficiency for planktonic bacteria (Del Giorgio and Cole, 1998), but is in
line with the modelled value of > 0.5 for the most productive
coastal and estuarine sites (Del Giorgio and Cole, 1998). Bacterial growth
efficiency is widely variable, both spatially and temporally, and the factors
that control it are not well understood. However, both the rate of supply of
organic substrate and its composition (bioavailable energy) seem to be
positively correlated with BGE, and it tends to increase from oligotrophic to
eutrophic environments (Del Giorgio and Cole, 1998). This is consistent with
high BGE in permeable sediments, which have a high input of fresh OC from
filtering during advective porewater flow (Ehrenhauss and Huettel, 2004), and
where a high proportion of bacterial cells may be active (as indicated by
higher biomass-specific uptake on the Ythan sand flat).
Finally, faunal uptake was relatively minor in the Ythan sand flat
experiment, and this suggests that bacterial C uptake may have been favoured
by a lack of competition from or grazing by macrofauna. A negative
relationship has previously been observed between macrofaunal biomass and
bacterial C and N uptake in the Arabian Sea, and a similar effect has been
observed in the Whittard Canyon (Hunter et al., 2012, 2013).
The short-term biological C processing patterns presented in Fig. 5 can
accommodate most observations in the literature, but some findings do not fit
in this conceptual scheme. For example, an experiment conducted in permeable
sediments of the Gulf of Gdansk does not show the expected bacterial
dominated biological C processing pattern. Instead it shows respiration
dominated biological C processing, with bacterial uptake responsible for only
16 % (Fig. 5). Further, an OC rich site with invasive mangroves in Hawaii
shows respiration dominated biological C processing, instead of an “active
faunal uptake” pattern (Fig. 5, Sweetman et al., 2010), due to mangrove
roots and detritus making the sediment inhospitable to macrofauna.
Finally, bacterial uptake dominated short-term biological C processing has
also been observed over 3 days in sediments from the Faroe–Shetland channel
at a depth of 1080 m (Gontikaki et al., 2011). This is considerably deeper
than all other observations, and the sediments contained a muddy fraction,
although also featuring grains up to gravel size. Thus this site does not fit
the same general description as others showing bacterial uptake dominated
biological C processing. In this case bacterial uptake dominated C processing
was observed over the initial 3 days of the experiment, and after 6 days
biological C processing was respiration dominated, in line with expectations.
The authors explained the initial rapid uptake of C by bacteria as a reaction
to the initially available reactive fraction of the added OM, before
hydrolysis of the remaining OC began in earnest (Gontikaki et al., 2011b). The
Porcupine Abyssal Plain also showed a change in short-term biological C
processing category between different experiment durations, showing an
unexpected active faunal uptake pattern after 60 h and the more expected
“respiration dominated” pattern after 192 and 552 h (Table 1). This was
explained as being due to the motility and selective feeding abilities of the
macrofauna, allowing them to initially outcompete bacteria. The majority of
studies which have included experiments of multiple short-term durations at
the same site have showed consistency of short-term biological C processing
patterns (Table 1; Witte et al., 2003; Bhuring et al., 2006; Woulds et al.,
2009); therefore, variation in experiment duration amongst the studies cited
is not thought to be a major driver of short-term biological C processing
patterns.
In summary, the proposed categorisation of short-term biological C processing
patterns works well across many different sites, but variation in
characteristics of individual sites can still lead to some unexpected
results.