Marine sediments, particularly those located in estuarine and coastal zones, are key locations for the burial of organic carbon (C). However, organic C delivered to the sediment is subjected to a range of biological C-cycling processes, the rates and relative importance of which vary markedly between sites, and which are thus difficult to predict.
In this study, stable isotope tracer experiments were used to quantify the processing of C by microbial and faunal communities in two contrasting Scottish estuarine sites: a subtidal, organic C rich site in Loch Etive with cohesive fine-grained sediment, and an intertidal, organic C poor site on an Ythan estuary sand flat with coarse-grained permeable sediments.
In both experiments, sediment cores were recovered and amended with
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 CO
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
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 CO
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.
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
Map showing site locations.
The Ythan estuary is a well-mixed estuary on the east coast of Scotland
(Fig. 1), 20 km north of Aberdeen. It is
The experimental set-up varied slightly between sites, to account for the differences in their depth and sediment grain size.
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
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
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
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
Fauna samples were oven-dried at 45
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
Overlying water samples were analysed for concentration and
Aliquots of sediment were treated with a Bligh and Dyer extraction, involving
shaking at room temperature in a
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
Carbon uptake by faunal groups was calculated by subtracting naturally
occurring
The DIC concentrations and
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
The mean recovery of added C from the bacterial, faunal and respired pools
together was 30
The average respiration rate of the added OC was similar in Loch Etive and on
the Ythan sand flat, and reached 0.64
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.
Macrofaunal biomass in the experimental cores was
4337
In Loch Etive, both faunal biomass and carbon uptake were dominated by two
ophuroids,
Taxa responsible for biomass and C uptake in
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
Bacterial biomass in the surface 5 cm of sediment in Loch Etive was
5515
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
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 CO
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
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
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
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
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.
Log
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).
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,
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
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
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
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.
The rate of respiration of added phytodetritus was dominantly controlled by temperature, rather than other factors such as benthic community biomass, sediment OC concentration, or solute transport mechanism.
Faunal C uptake was related to faunal biomass. Further, total biological C processing rates in this and previous studies appear to be dominantly determined by benthic biomass. Therefore benthic community structure has a role in controlling the C processing capacity of benthic environments.
A new biological C processing pattern category was proposed to be titled “bacterial uptake dominated”, which seems usually to be observed in permeable sediments, where conditions are particularly conducive to active bacterial populations.
Data associated with this work are available from the Research Data Leeds
repository under a CC-BY license at:
C. Woulds designed and conducted the experiments with input from G. Cowie, J. Middelburg, and U. Witte. Sample analysis was completed by C. Woulds, S. Bouillon, and E. Drake. C. Woulds prepared the manuscript with the assistance of all co-authors.
The authors would like to thank Eva-Maria Zetsche, Val Johnson, Owen McPherson, Caroline Gill, and Gwylim Lynn for assistance with the Ythan sand flat fieldwork, and Matthew Schwartz, Rachel Jeffreys, Kate Larkin, Andy Gooday, and Christine Whitcraft for assistance with the Loch Etive fieldwork. Jonathan Carrivick created Fig. 1. The work was funded by the Natural Environment Research Council and the Netherlands Earth System Science Center. We would also like to thank two anonymous reviewers for their comments which helped to improve the manuscript. Edited by: C. Heinze