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Carbon oxidation in sediment inhabited by Nereis spp. and Arenicola marina
- Impact of polychaetes (Nereis spp. and Arenicola marina) on carbon biogeochemistry in coastal marine sediments

Carbon oxidation in sediment inhabited by Nereis spp. and Arenicola marina

Impact on microbial reaction rates

The first studies examining the importance of Nereis spp. and Arenicola marina on sediment processes focused on the role of these animals for sediment–water fluxes and vertical porewater profiles of various solutes. [41-43] These studies were supplemented with measurements of e.g. burrow architecture and defecation rates.[12,19] More recent biogeochemical studies employing a variety of experimental and modelling techniques have gained important new knowledge on the mechanisms controlling reaction rates in bioturbated sediments in general[23,44] and more specifically in nearshore sediments affected by Nereis spp. and Arenicola marina.[9,45,46]


Irrigation is particularly important in enhancing solute exchange between overlying water and pore fluids.[22] However, it is not an easy task to measure the impact of infauna on solute fluxes in nature due to the obvious lack of fauna-free sediment patches comparable to bioturbated locations. Sieving and homogenizing sediment to remove fauna and other inhomogeneities have partly solved this problem. Measurements are then done in laboratory microcosms by reintroducing known densities of animals, while defaunated controls are kept as a reference.[42] Despite its inherent limitations (see later), this technique has been and still is widely used for certain purposes.[9,45] Other studies use intact sediment microcosms, which are deoxygenated by N2 flushing in order to force the existing fauna out of the sediment followed by introduction of known densities of selected species when aeration is resumed.[47] Unfortunately, only few studies have made comparable in situ measurements without manipulations, and few or none have yet been published for Nereis spp. and Arenicola marina.

Although the above-mentioned manipulative techniques are problematic, they have provided valuable information on the potential impact of burrow dwelling worms on total sediment metabolism. It has been shown that Nereis spp. stimulates benthic metabolism in manipulated sediment, measured as O2 uptake or CO2 production, by 45 to 179% compared with defaunated sediments (Table 3). Furthermore, in a study where homogenized sediment microcosms with Nereis virens (600 m-2) were combined with flowmeter measurements on individual worm + burrow systems, Kristensen[42] found that the diffusive flux across burrow walls accounted for 31% of the total oxygen uptake, while only 11% was consumed by Nereis virens itself. Diffusive flux across the sediment/water interface accounted for the remaining 58% of the oxygen uptake.

Only few attempts have been made to determine the flux enhancement by A. marina under manipulated laboratory conditions. The few data available indicate that this species have a higher capacity to increase fluxes than Nereis spp. Upward percolation of irrigated water through the feeding funnel forces porewater rich in solutes out of the sediment, which is more efficient than the combined action of radial diffusion into the burrow and advective transport out of the burrow as in the Nereis case.[54]

The faunal induced flux enhancement reported from manipulated non-steady laboratory systems are not comparable to in situ conditions as evidenced from the much lower (10 and 25%, Table 3) enhancement by Arenicola marina and Nereis diversicolor under natural conditions.[46,52] The degree of flux stimulation by benthic infauna is therefore highly dependent on the type of sediment manipulation made, and the measured flux enhancement does not always reflect true changes in microbial activity.[54] A significant part of fluxes is rather caused by porewater flushing, i.e. removal of porewater CO2 or sulfide (reducing equivalents with subsequent reoxidation at the surface) via infaunal irrigation. This is particularly true in experiments using homogenized or otherwise defaunated sediment, where animals are added several days after the establishment of sediment microcosms. CO2 or reducing equivalents produced by microbial metabolism within the sediment during such long conditioning period tends to accumulate in the porewater. Immediately after addition of infauna such as Nereis spp, these porewater solutes are rapidly transported into the newly established burrows and carried to the overlying water by the irrigation current. A recent study has shown that the transport of porewater solutes into burrows is dominated by radial diffusion in impermeable fine-grained silty sediments, while porewater advection is more important in permeable sandy sediments.[53] As a consequence, the flux is extremely high initially and first approaches steady state gradually after a time period of typically 1–2 weeks[47] (Fig. 9). The removal of dissolved metabolites from the porewater is clearly evident as significantly lowered concentrations when vertical profiles of e.g. CO2 in bioturbated sediment are compared with defaunated sediment (Fig. 10).

Organic matter replenishment is another problem with the manipulated laboratory experiments. The microcosms are rarely continuously supplied with new organic substrates to balance the removal by decomposition. Even the supply from benthic diatoms may be impaired as the experiments usually are performed in darkness. As a consequence, true steady state will never be reached. The stable flux conditions usually observed after the initial porewater flushing (Fig. 9) can therefore only be considered a short-term pseudo steady state. In due course (months), fluxes must decrease to very low levels, and eventually be lower in bioturbated than defaunated sediment due to exhaustion of reactive organic matter.

Decomposition rates

The flux enhancement reached in manipulated systems, when the pseudo steady state is approached immediately after the initial porewater flushing, should be considered a measure of the enhanced metabolic capacity of all heterotrophic organisms in the sediment.[55] However, this proposition is difficult to test experimentally under natural conditions because defaunated sediments underlying oxic water columns are rare. An alternative approach is to apply a speculative scenario based on the current knowledge on effects of Nereis spp. and Arenicola marina.

The frame of scenario is a hypothetical marine sediment environment, with no temporal (seasonal and diurnal) variability, which is supplied continuously with organic carbon from above by deposition on the surface. The environment consists of two previously fauna-free, but adjoining sites: To one site a population of Arenicola marina is introduced whereas the other remains defaunated. They both receive the same quantity and quality of organic input (dGi/dt) (Fig. 11). Thus, the deposit-feeding A. marina is not assumed to increase organic carbon deposition (see later). The bulk decomposition rate within the sediment is assumed to be first-order with respect to the reactive organic carbon content: dG/dt = k G, where k is the first-order decomposition coefficient (decomposition capacity) and G is the inventory of reactive organic carbon. [56]A. marina is assumed to enhance the capacity for organic matter decomposition, and thus to increase the decomposition coefficient compared with the defaunated sediment, i. e. kb > ku. Initially (just after introduction of A. marina), the total metabolism of the faunated (dGb/dt = kbGu) system is kb/ku times higher than that of the defaunated system (dGu/dt = kuGu) because the reactive organic inventory Gu is similar in both systems. In this situation, the enhanced decomposition due to A. marina is independent of the organic input, and simulates the above mentioned manipulated laboratory experiments when the initial porewater flushing has ceased. Hence, in their manipulated system, Kristensen and Blackburn[54] found that the enhanced decomposition capacity (kb/ku, based on measured disappearance of particulate organic carbon) of 2.6 in the presence of Nereis virens actually was similar to the enhanced oxygen uptake (factor 2.5) just after the initial flushing period.

However, the present model approach (Fig. 11) predicts that the amount of organic carbon mineralization at steady state must be equivalent to that being supplied (ignoring permanent burial), irrespective of the presence of A. marina: dGb/dt = dGu/dt = dGi/dt. The steady state pool of reactive organic carbon in the faunated sediment must then be lower than in the defaunated sediment in proportion to the ratio between decomposition coefficients: Gb = ku/kbGu. Basically, the difference between the two systems is an increased decomposition capacity (i.e. the decomposition coefficient, k) in the faunated system and thus a decreased total pool of reactive organic carbon at steady state compared with a defaunated system (Fig. 12), while the bulk decomposition rate and flux are similar at both sites (see A. marina under in situ conditions in Table 3).

Decomposition must be increased when the faunal activities enhance deposition of organic matter to the sediment, whereas the organic pool may reach a level higher than, similar to or lower than in the defaunated sediment, depending on the functional type, density and size of animals present. In a very illustrative experiment, Christensen et al.[9] examined the impact of suspension-feeding N. diversicolor and non-suspension-feeding N. virens on carbon dynamics in organic-poor sediment when exposed to phytoplankton in the overlying water. The presence of phytoplankton resulted in a 30-fold higher deposition (clearance, Fig. 13) of particulate carbon to the sediment inhabited by N. diversicolor than to N. virens and defaunated sediment. Concurrently, oxygen uptake was increased by a factor of 3 in sediment with N. diversicolor, but only a factor of about 1.5 in N. virens and defaunated sediment (Fig. 14).

About 30% of the deposited carbon in the N. diversicolor sediment was oxidized and lost rapidly as excess CO2 flux to the water column. Incorporation into N. diversicolor tissues accounted for 45% of the carbon, while the remaining accumulated within the sediment. In the N. virens sediment, where no excess phytoplankton deposition occurred, decomposition resulted in a net loss of sedimentary carbon due to the enhancement of microbial decomposition by N. virens. Thus, two almost identical species may either enrich or impoverish the organic inventory of sediments depending on their life habit.

The intense reworking activity of conveyor-belt feeders like Arenicola marina results in subduction of surface sediment at rates significantly higher than natural sedimentation rates. As a consequence, benthic microalgae and other labile or digestible organic particles (e.g. bacteria) are drawn into subsurface layers of the sediment. Thus, Retraubun et al.[57] observed similar concentrations of benthic diatoms in the feeding funnel and feeding pocket of A. marina than at the sediment surface. These reactive organic substrates not only serve as nutrition for the worms, but also displace microbial decomposition within the sediment. The typical exponential decrease in anaerobic carbon oxidation with depth in sediments affected by passive sedimentation is replaced by lower surface rates and only gradually decreasing rates with depth within the bioturbated depth of intensively reworked sediments (Fig. 15). The total rate of microbial activity integrated within the bioturbated depth may not change significantly by the displacement of organic matter and microbial processes. However, the trough frequently created by the feeding funnel of A. marina may act as a subduction trap for detritus swept horizontally along the sediment surface by currents and waves,[43] and thus enhance both the inventory of organic substrates as well as the total depth integrated benthic metabolism. Under these circumstances, the crude assumptions and the general conclusions made in the model for A. marina discussed above do not hold. Anyway, the model still provides a basic understanding of the balance between reaction rates and the inventory of reactive organic matter in sediments affected by burrowing fauna.

Causes for stimulated microbial decomposition

A number of macrofaunal activities are known or have been inferred to cause the enhancement of microbial metabolism and capacity for organic matter degradation in bioturbated sediments:[23] particle manipulation, grazing, excretion/secretion, burrow/tube construction, irrigation and particle reworking. The two latter activities, which are the focus of this paper, are considered particularly important controlling factors for carbon diagenesis in Nereis spp. and Arenicola marina inhabited sediments.[4,55]

The current knowledge on the underlying mechanisms for the impact of irrigation (defined here as downward transport of oxidants and upward transport of metabolites in sediments) and particle reworking (defined here as transfer of organic matter and redox sensitive minerals between redox zones) by species like Nereis spp. and A. marina on carbon diagenesis in coastal sediments will be summarized in the following. While acknowledging the simultaneous and inseparable nature of these activities, they will be treated individually and compared within and between species, when possible.

The role of oxygen

A number of studies have emphasized that aerobic and anaerobic decomposition are comparable for fresh and reactive organic substrates, while aerobic processes proceed much faster for partly degraded and refractory compounds.[34,58,59] In an experiment where carbon mineralization of 14C labelled fresh and aged diatoms (Skeletonema costatum) and barley hay (Hordeum vulgare) was followed for about one month, Kristensen and Holmer[59] showed that the initial decay of fresh materials occurs at almost the same rate in both oxic and anoxic sediment (Fig. 16). After ageing, degradation is 5 to 10 times faster under oxic than anoxic conditions. Based on these and similar results it has been argued that introduction of oxygen into anoxic sediment by macrofaunal irrigation or translocation of organic matter from anoxic to oxic environments by particle reworking promotes decomposition of organic matter in sediments.[44,59]

Quantitative estimates of the enhanced decomposition caused by injection of oxygen into actively irrigated burrows or by oxygen exposure due to particle reworking are rare.[55] By the use of a modified version of the simple volumetric model presented by Kristensen and Holmer,[59] rough estimates can be provided for the stimulated carbon reaction rate in sandy coastal sediment shortly after the introduction of macrobiotic activity in the form of either irrigated burrows of e.g. Nereis diversicolor or burrows reworked by e.g. Arenicola marina.

In both cases, the calculations are based on the following common assumptions: (i) all diagenetic processes occur in the upper L cm of the sediment column; (ii) the oxic surface zone is Lox cm thick; (iii) the rate of deposition (e.g. phytoplankton) or production (e.g. benthic diatoms) at the sediment surface of labile organic matter is similar irrespective of the species present; (iv) the fresh and labile detritus is mineralized A1 times faster (both in the presence and absence of oxygen) than the old and partly degraded detritus in the anoxic zone (R1ox = R1an = R1 = A1 R2an); (v) mineralization of old and partly degraded organic matter from anoxic zones is enhanced by a factor of A2 when exposed to oxygen at the surface during reworking or along irrigated burrow walls (R2ox = A2R2an); (vi) no depth dependent change in degradability of sediment detritus occurs in oxic and anoxic zones (dR/dx = 0), and the anoxic mineralization rate is independent of electron acceptors.

In the Nereis diversicolor irrigation model (Fig. 17(a)) the following specific conditions are assumed: (i) all fresh and labile detritus deposited at the surface is located in the oxic surface layer; (ii) the N. diversicolor abundance is d individuals m-2 ; (iii) burrows are U-shaped with two openings at the surface and a total length of Lb cm and a radius of r cm; (iv) irrigation is continuous and the oxic zone around burrows is permanently Box cm thick. By relating volumes with reaction rates in the various zones, total sediment carbon oxidation m-2 in the presence and absence of irrigated burrows with oxic walls can be estimated according to eqn. (5) (irrigated) and (6) (defaunated):

Ciox = R2an (V - (Vox + Vban + Vwox)) + R1 (Vox - Vbox) + R2ox Vwox     (5)

Cdox = R2an (V - Vox)+ R1Vox     (6)

where: V = L × 104 is total sediment volume (cm3 m-2) to depth L; Vox = Lox × 104 is volume oxic surface sediment without burrows; Vban = π r2(Lb - 2Lox) d is subsurface burrow lumen volume; Vbox = π r2 2Lox d is surface burrow lumen volume; Vwox = π (Box 2 + 2r Box) (Lb - 2Lox) d is oxic subsurface burrow wall volume. The initial enhancement of carbon oxidation caused by the presence of irrigated burrows with oxic walls is then, Ei = Ciox/Cdox.

In the reworking case with Arenicola marina (Fig. 17(b)) the following specific conditions are assumed: (i) reworking is continuous and subsurface sediment is distributed in an even layer on top of the sediment with a steady state thickness at least similar to the depth of the oxic surface layer (Lox); (ii) labile surface sediment with a thickness similar to that in the defaunated situation (L1 = Lox) is continuously pushed downward into the anoxic zone; (iii) the A. marina abundance is d individuals m-2; (iv) since burrows are assumed vertical and the presence of oxic subsurface sediment (e.g. burrow walls) is ignored, the burrow lumen can be excluded from calculations (these assumptions are clearly false, but necessary, when only reworking activities are considered). From sediment volumes and reaction rates in the various zones, total sediment carbon oxidation (m-2) in the presence and absence of sediment reworking can be estimated according to eqn. (7) (reworked) and (8) (defaunated), where the volume of reduced subsurface sediment deposited at the oxic surface (Vrox) is similar to the volume of buried sediment containing labile detritus (V1).

Crox = R2an (V- (V1 + Vrox)) + R1V1 + R2ox Vrox     (7)

Cdox = R2an (V - Vox)+ R1 Vox     (8)

where: V = L × 104 is total sediment volume (cm3 m-2) to depth L; Vox = Lox × 104 is volume oxic surface sediment without burrows; V1 = L1 × 104 cm3 m-2 is volume of buried sediment containing labile detritus; Vrox = Lox × 104 cm3 m-2 is volume of reduced subsurface sediment deposited at the oxic surface. However, due to the continuous input of labile detritus and deposition by reworking a dilution of the labile material into a larger sediment volume obviously occurs. Nevertheless, based on the assumption above, the volumetric reaction rate should remain unaffected. The initial enhancement of carbon oxidation caused by sediment reworking are then, Er = Crox/Cdox = (L + (A1+ A2 - 2)Lox)/(L + ((A1 - 1) Lox).

In the irrigation model (eqn. (5) and (6)), the variables L, Lb, Lox, r, Box, A1 and A2 may all change depending on factors like season, sediment type and worm size. However, for simplicity we have chosen to keep them all constant: L = 20 cm; Lb = 20 cm; Lox = 0.3 cm; r = 0.3 cm; Box = 0.2 cm; A1 = 20; A2 = 10. These fixed values are chosen based on past and present experience on nereid polychaetes[10,60] and sediment biogeochemistry in shallow sandy areas.[61] By varying d, our model predicts that the degree of stimulation is directly proportional to worm abundance, when the oxic zone around burrows is assumed independent of the distance between burrows (Fig. 18). Accordingly, the enhancement of total sediment carbon oxidation due to 2000 irrigated burrows of N. diversicolor (m-2) is estimated to Ei = 1.61. This is within the previously mentioned range of published enhancements of benthic metabolism caused by a similar abundance of these animals. However, as the worm abundance increases, the anoxic to oxic volume of subsurface sediment and thus the production and reoxidation of reduced metabolites decrease. The oxic zone around burrows may therefore expand, resulting in a proportionally larger oxic volume at high abundances, and thus larger impact of irrigated burrows on sediment decomposition. The upper limit is reached at hypothetically high abundances when all subsurface sediment is converted to oxic burrow walls.

The reworking model (eqn. (7) and (8)) predicts that carbon oxidation in the presence of A. marina is enhanced by Er = 1.11, when the variables, L, Lox, A1 and A2 are similar to those used in the irrigation model, and that the enhancement is independent of worm abundance, d (Fig. 18). This prediction is only valid when reworked subsurface sediment containing reactive organic material covers the sediment surface to a depth similar to the oxic zone and that reaction rates are not so fast as to eliminate entirely the organic material exposed in a single transit. This means that below a certain threshold the enhancement must be proportional to abundance. As one average sized individual deposits 1.4 × 10-3cm d-1 sediment at the surface,[19] a population size of 7 m-2 is needed to deposit a 0.3 cm layer (equivalent to Lox) every month. The actual threshold of abundance is probably lower than this limit, since there were no signs of changes in reactivity of aged materials exposed to oxygen for one month.[60]

It is important to note that these model calculations are only valid for the initial conditions after introduction of macro-benthic activity. For a fixed influx of material, the steady state mass of reactive organic matter in a sediment deposit where decomposition rates are enhanced by faunal activities must be lower than for a defaunated situation (see the "Decomposition rates" sub – section above). Nevertheless, these model examples clearly illustrates that decomposition capacity of partly degraded organic matter along oxic walls of irrigated infaunal burrows is enhanced progressively more than by exposure of subsurface sediment to oxygen during reworking.

In the reworking case, where A. marina is used as model organism, oxygen effects due to irrigation of this worm are ignored. As mentioned earlier, the burrow structure and irrigation type of A. marina may result in comparable or larger impact on sedimentary reaction rates than that of N. diversicolor, and should be recognized and included in sedimentary budget predictions. As a consequence, the overall impact (including both reworking and irrigation) of A. marina may very well be higher than of N. diversicolor. Accordingly, Banta et al.[45] reported up to 3-fold higher stimulation of carbon oxidation by A. marina than N. diversicolor.

The oxygen effect of bioturbation on reaction rates in sediments may be masked by other, and in this context, less known factors. Recently, Mikkelsen and Kristensen[62] conducted an experiment, where fresh and aged (after 55 day aerobic decay) 14C labelled fucus serratus detritus was placed at the oxic surface or buried into anoxic subsurface layers of N. diversicolor bioturbated and defaunated sediment. According to the propositions made above, it was expected that degradation of fresh detritus would proceed at similar rates irrespective of its position within the sediment and the presence of N. diversicolor. Degradation of aged detritus, on the other hand, should be strongly stimulated by irrigation activities of N. diversicolor when buried into anoxic sediment. The results showed, as expected, that the carbon mineralization of refractory detritus buried in anoxic sediment only proceeded at 28% of the rate of detritus deposited at the oxic surface (Fig. 19). It was surprising, though, that mineralization of labile detritus was reduced to half (53%) when buried in anoxic sediment. The presence of N. diversicolor always enhanced carbon mineralization of added detritus. The effect was modest for surface-deposited detritus (25–54%) and was probably caused by feeding, assimilation and respiration by the worms. Mineralization of subsurface-deposited detritus was increased dramatically (155% for labile detritus and 392% for refractory detritus), reaching a level comparable to the corresponding treatments with surface-deposited detritus. The more than twofold difference in stimulation between the two types of detritus must be caused by the stronger oxygen effect on decay of refractory detritus. The unexpected large decrease in mineralization of subsurface-deposited labile detritus and subsequent increase in the presence of N. diversicolor must be caused by other factors than oxygen availability. A plausible explanation for this discrepancy may be inhibition of microbial activity by accumulation of noxious metabolites in defaunated subsurface sediments, and subsequent alleviation in the presence of irrigating infauna.[23]

Removal of metabolites

Irrigation not only promotes metabolic processes by supplying electron acceptors, like oxygen, to bioturbated subsurface sediments, but also net reactions in anoxic regions of inhabited sediments are stimulated.[63] This implies that net rates of anaerobic microbial processes are controlled by the exchange of other solutes than oxygen during irrigation. Metabolites, such as CO2, ammonium and sulfide ions (Fig. 10) in particular, are efficiently removed from sediment porewaters by infaunal irrigation.

It was a puzzle for years to understand why the total CO2 release from the sediment in defaunated microcosms of different thickness, but containing the same sediment type, was almost independent of sediment thickness. As a consequence, the volume specific net mineralization must be inversely related to sediment thickness (Fig. 20). Recently, Aller and Aller[23] convincingly showed that net mineralization rates increase dramatically as diffusion scale (sediment thickness) decreases and efficiency of solute exchange with overlying water increases. This demonstrates that irrigation of sediment may result in an infaunal density-dependent increase in mineralization, microbial activity and sediment-water solute fluxes of constituents not normally considered sensitive to concentration dependent reactions. The effects are relatively modest (1.5–2.0 times) for diffusion distances larger than 1 cm, but become increasingly important at small scales (Fig. 20). Thus, anaerobic mineralization of organic matter increases with increasing diffusive exchange or, in other words, macrofaunal burrow spacing and irrigation intensity.

The dependence of reaction rates on diffusion scale presumably reflects the balance between competing reactions and processes that vary as a function of concentration of reactants, products, or inhibiting constituents. Aller and Aller[23] considered three possible cases as representative examples capable of explaining the observed reaction rate–diffusion scale patterns: (i) coupled mineralization–biological uptake, where the balance between a constant rate of nutrient mineralization and a concentration dependent (Michaelis–Menten kinetics) assimilation favours a high net mineralization at small diffusion scales (Fig. 21); (ii) coupled mineralization–abiogenic precipitation, where assimilation from case (i) is substituted with concentration dependent precipitation reactions. Thus progressively higher removal of solutes (e.g. CO2) is due to precipitation (e.g. carbonates) when the diffusion scales become larger; (iii) mineralization–inhibiting metabolite interactions, where the response of mineralization activity to transport scale results from removal of inhibiting metabolites (Fig. 22). As transport scale decreases, the concentration of metabolic products and reaction inhibitors must also decrease, resulting in an overall increase in mineralization rate at a fixed value of biomass. If relaxation of inhibitory effects enhances microbial growth, mineralization may also change as a result of the higher reaction capacity by the increased biomass under more favourable conditions.

The proposed effect of infauna on metabolite dependent processes has not yet been confirmed from direct measurements in bioturbated sediments. However, relaxation of metabolite effects is a very plausible contributing explanation for the observed irrigation effect of Nereis spp. and Arenicola marina on benthic carbon mineralization.

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