BIOTURBATION. Introduction. Particle Bioturbation
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1 BIOTURBATION D. H. Shull, Western Washington University, Bellingham, WA, USA & 29 Elsevier Ltd. All rights reserved. Introduction Activities of organisms inhabiting seafloor sediments (termed benthic infauna) are concealed from visual observation but their effects on sediment chemical and physical properties are nevertheless apparent. Sediment ingestion, the construction of pits, mounds, fecal pellets, and burrows, and the ventilation of subsurface burrows with overlying water significantly alter rates of chemical reactions and sediment water exchange, destroy signals of stratigraphic tracers, bury reactive organic matter, exhume buried chemical contaminants, and change sediment physical properties such as grain size, porosity, and permeability. Biogenic sediment reworking resulting in a detectable change in sediment physical and chemical properties is termed bioturbation. It is critical to account for bioturbation when calculating chemical fluxes at the sediment water interface and when interpreting chemical profiles in sediments. In the narrowest sense, bioturbation refers to the biogenic transport of particles that destroys stratigraphic signals. In the broader sense it can refer to biogenic transport of pore water and changes in sediment physical properties due to organism activities as well. Bioturbation and its effects on sediment chemistry and stratigraphy is a natural consequence of adaptation by organisms to living and foraging in sediments. Particle Bioturbation Deposit feeding, the ingestion of particles comprising sedimentary deposits, is the dominant feeding strategy in muddy sediments. In fact, since the vast majority of the ocean is underlain by muddy sediments, deposit feeding is the dominant feeding strategy on the majority of the Earth s surface. Because digestible organic matter typically comprises less than 1% of sediments by mass, to meet their metabolic needs deposit feeders exhibit rapid sediment ingestion rates, averaging roughly three body weights per day. Deposit feeders adapted to living in sediments with relatively low organic matter concentrations tend to exhibit elevated ingestion rates; there is no free lunch even for deposit feeders. Rates of deposit feeding of individual organisms increase with increasing body size so that bioturbation rates in some sedimentary deposits may be controlled by a handful of larger species. Deposit feeders employ a wide variety of strategies to collect particles for food, but reworking modes due to deposit feeding can be broken down into the following categories: conveyor-belt feeding where particles are collected at depth and deposited at the sediment surface; subductive feeding, where particles are collected at or near the sediment surface and deposited at depth; and interior feeding where particles are collected and deposited within the sediment column. These feeding modes transport particles the length of the organism s body or the length of its burrow. Some species of deposit feeders also ingest and egest sediment near the sediment surface, resulting in horizontal movement of particles but limited vertical displacement. Due to rapid particle ingestion rates and relatively large horizontal and vertical transport distances, deposit feeding is considered to be the primary agent of bioturbation. Benthic organisms also rework sediments through burrow formation. Muddy sediments behave more like elastic solids than granular material. A benthic burrower in muddy sediments uses its burrowing apparatus (bivalve foot, polychaete proboscis, amphipod carapace, or other burrowing tool) like a wedge to create and propagate cracks in sediments. After an organism passes through a crack, sediments tend to rebound viscoelastically resulting in relatively little net movement of particles compared to deposit feeding. An exception to this generality is burrowing by large epibenthic predators including skates, rays, and benthic-feeding marine mammals such as gray whales and walrus, which can cause extensive reworking in sediment patches where they are feeding. From a particle s perspective, bioturbation consists of relatively short-lived intervals of particle movement due to deposit feeding or burrowing interspersed by relatively long periods during which the particles remain at rest. When particles pass through animal guts, in addition to changing location, the particles may be aggregated into fecal pellets (particles surrounded by or embedded in mucopolymers). When constructing burrows, some infauna produce mucopolymer glue to form sturdy burrow walls, locking particles into place for an extended period of time. Transport of subsurface particles to the sediment surface by conveyor-belt feeding results in downward gravitative movement of particles within the sediment column as subsurface feeding voids are 395
2 396 BIOTURBATION filled with sediment from above. Within a particular sedimentary habitat many particle reworking mechanisms occur simultaneously. There are many ways to quantify mathematically the ensemble of particle motions that results in bioturbation. Traditionally, bioturbation has been modeled as though it were analogous to diffusion. This means that the collection of particle motions resembles a large number of small random displacements. Under these assumptions, bioturbation is included in the general diagenetic equation as a biodiffusion coefficient, D B. Ignoring vertical gradients in porosity and sediment compaction, the rate of change of a chemical tracer, C, in the vertical spatial dimension, x, can be represented as follows: Table 1 Variation in the biodiffusion coefficient, D B, sedimentation rate, u, and the Peclet number, Pe, characteristic of different benthic environments. A Peclet number greater than 1 indicates sediment accumulation is more important than bioturbation D B u L Pe Shallow water Cont. Shelf Slope Deep sea A Peclet number less than 1 indicates that bioturbation is more important for transport relative to ¼ 2 C þ X R; xol ½1Š where D B is the biodiffusion coefficient (cm 2 yr 1 ), P u is the sediment accumulation rate (cm yr 1 ), and R represents the sum of chemical reactions. In the absence of specific information on bioturbation mechanisms, it is often assumed that D B is constant throughout the reworked layer to the depth L. Below the depth L, D B is zero. The advantage of this formulation is that all the various particle reworking processes are quantified by one parameter, D B. The nondimensional Peclet number, Pe ¼ uld 1 B, quantifies the relative importance of bioturbation and sediment accumulation in determining the profile of C within the reworked layer. Values of Pe less than 1 indicate a strong influence of bioturbation. Table 1 summarizes the general pattern of variation in D B, u, L, and Pe among benthic provinces at different water depths. The depth of the reworked layer, L, shows little systematic variation among habitats, averaging 1 cm. Although we would expect considerable variation in Pe, the low values in each province indicate that bioturbation is generally important throughout the ocean. An easy-toremember rule of thumb regarding bioturbation rates is that D B varies from c..1 to 1 cm 2 yr 1 from deep-sea to shallow-water depths. This variation is correlated with increased abundance of infauna, greater rates of food supply, and (with the exception of polar regions) elevated average bottom-water temperatures with decreasing water depth. Because bioturbation mechanisms can transport particles relatively large distances, roughly the length of the reworked zone, L, and because particle trajectories are often nonrandom, the biodiffusion coefficient is not appropriate for modeling the effects of bioturbation on transport of some tracers. A more general model of particle mixing that includes longer-distance, nonrandom particle trajectories is the nonlocal bioturbation model. Again neglecting variation in porosity: Z ¼ Kðx ; x; tþcðx Þdx CðxÞ Z L Kðx; x ; tþdx þ X R ½2Š where K is the exchange function (dimensions: time 1 ) that quantifies the rate of particle movement from one depth, x, to any other depth, x. The first term on the right-hand side gives the concentration change at depth x due to the delivery of a particle tracer from other depths, x. The second term gives the concentration change at depth x due to transport of a tracer from depth x to other depths x. The other terms are defined as in eqn [1]. The exchange function, K, can potentially quantify a complex ensemble of bioturbation mechanisms. Analogs of eqn [2] that rely on discrete mathematics exist. In one dimension, nonlocal transport can be modeled as a transition matrix in which the rows of the transition matrix correspond to depths in the sediment and the matrix elements quantify the probability of transport of a tracer among depths. Multiple-dimensional automaton models can simulate complex modes of particle transport in both vertical and horizontal dimensions. These more complex models can better capture the complexities of bioturbation but sacrifice the one-parameter simplicity of eqn [1]. There are two common approaches for determining the values of the bioturbation parameters in these models. Mixing parameters can be estimated from direct measurements of deposit-feeder ingestion rates and organism burrowing rates. More often, these parameters are estimated by measuring sedimentbound tracers with known inputs to the sediment and
3 BIOTURBATION 397 known reaction rates ( P R). Mixing parameters are then calculated by fitting measured tracer profiles to profiles calculated by use of the appropriate mathematical model. Useful bioturbation tracers include excess activities of naturally occurring particlereactive radionuclides such as 234 Th, 21 Pb, or 7 Be. These radionuclides have a relatively continuous source either from the atmosphere or from the overlying water column, are rapidly scavenged onto particles, and sink to the seafloor (see Sediment Chronologies). In addition, chlorophyll a, artificial tracers added to the sediment surface as an impulse such as glass beads or fluorescent luminophores, or other exotic identifiable material with a known rate of input are used as tracers of bioturbation. The profile of excess 21 Pb in Figure 1 illustrates several effects of bioturbation on a tracer profile. The rate of bioturbation in the top 6 cm is rapid enough to completely mix excess 21 Pb within this layer. The subsurface peak at cm indicates subsurface deposition of surficial material. Below 16 cm, the slope of the profile is set by the rate of sediment accumulation and radioactive decay of 21 Pb. Bioturbation has important consequences for sediment stratigraphy, chemistry, and biology. Bioturbation can homogenize tracers within the reworked layer (Figure 1). Bioturbation acts as a low-pass filter, destroying information deposited on short timescales, but preserving longer-term trends. Bioturbation makes it generally difficult or impossible to resolve timescales of less than 1 3 years stratigraphically in deep-sea sediment cores. If the bioturbation mechanism is not known, it is difficult to separate changes in the input signal from changes due to mixing (Figure 2). If mixing is not complete, and the bioturbation mechanism is known, it may be possible to deconvolve the input signal to the stratigraphic record, although detailed information will be lost. If bioturbation in the surface reworked zone completely homogenizes a tracer, then knowing the mixing mechanism is unimportant. Once pancake batter is thoroughly mixed, for example, it no longer contains information on how the mixing was performed. Bioturbation has important consequences for sediment geochemistry. Bioturbation buries reactive organic matter. Subductive deposit feeders selectively feed on organic-rich particles near the sediment surface and deposit them at depth, perhaps as food caches. In the presence of horizontal transport of organic matter, or suspension-feeding benthos that locally enhance organic matter deposition through biodeposit formation, bioturbation can greatly enhance the organic matter inventory in sediments. Burial of organic matter exposes it to different oxidants, changing the degradation pathway. In particular, reworking of Mn and Fe oxides cycles them between oxidative and reducing environments, Excess 21 Pb (dpm g 1 ) Well-mixed surface layer 5 Tracer concentration Depth (cm) Subduction of surficial 21 Pb Sediment accumulation below reworked layer Depth (cm) Figure 1 Excess 21 Pb activity vs. depth in a sediment core from Narragansett Bay, Rhode Island. Data with permission from Shull DH (21) Transition-matrix model of bioturbation and radionuclide diagenesis. Limnology and Oceanography 46(4): Copyright (21) by the American Society of Limnology and Oceanography, Inc. 3 Figure 2 Changes in the profile of a hypothetical conservative tracer present initially as two narrow subsurface peaks, as predicted from eqn [1]. D B ¼.1 cm 2 yr 1, u ¼.1 cm yr 1, L ¼ 1 cm. Solid line: tracer profile at t ¼. Dotted line: t ¼ 25 years. Dashed line: t ¼ 15 years.
4 398 BIOTURBATION resulting in enhanced anaerobic degradation of organic matter. Bioturbation changes sediment properties as well. Pelletization changes the sediment grain size distribution. Furthermore, bioturbation rates are particlesize-dependent. Size-selective feeding by deposit feeders results in biogenic graded bedding with lag layers of large sediment particles either at the sediment surface or at depth, depending upon the bioturbation mechanism. Formation of pellets and burrows increases sediment porosity, counteracting the effects of sediment compaction. Sediment surface manifestations of bioturbation such as pits, mounds, and tubes alter seafloor roughness and flow characteristics of the benthic boundary layer, roughly doubling the drag compared to a hydrodynamically smooth bed. Pore-Water Bioirrigation Most benthic infauna maintain a burrow that connects to the sediment water interface to facilitate respiration, feeding, defecation, and other metabolic processes. These burrows exist in a range of geometries including vertical cylinders, U- or J-shaped tubes, or branching networks. In deep-sea sediments, dissolved oxygen can penetrate 3 m into the sediment. Near the shore, however, oxygen penetration is quite variable and in muddy sediments it often penetrates no farther than a few millimeters. To meet their metabolic requirements for oxygen, infauna ventilate their burrows by thrashing their bodies, flapping their appendages, by peristalsis, by beating cilia, or by oscillating like pistons in their tubes. These ventilation mechanisms result in intermittent burrow flushing, which exchanges a portion of the fluid inside the burrow with overlying water. In this way, organisms in the sediment can flush out metabolic wastes and toxins such as hydrogen sulfide that have accumulated in their burrows and they can restock the burrow water with dissolved oxygen. Observations of organisms in artificial tubes maintained in the laboratory indicate that burrow ventilation is episodic, with ventilation frequencies ranging from once per hour to 1 or more ventilation events per hour. Deposit-feeding infauna generally ventilate less frequently than suspension-feeding infauna, which pump water through their burrows for both respiration and food capture. The sediments into which these burrows are built are mixtures of particles and interconnected pore water. Surficial sediments may possess porosities (defined as the volume of interconnected pore water per unit volume of sediment) in excess of 9%. Thus, surface sediments generally contain more pore water than particles. The rate of molecular diffusion of solutes through pore water is reduced relative to diffusion in a free solution because the solutes must follow a winding path through the particles, called sediment tortuousity. Particle bioturbation mechanisms redistribute this pore water along with the particles, but since rates of pore-water transport, inferred from dissolved tracer distributions, are typically an order of magnitude higher than rates of particle bioturbation, particle reworking is a relatively unimportant mechanism for transporting pore water. Rather, burrow ventilation seems to be the most important biogenic mechanism of pore-water transport. The consequences of burrow ventilation on pore-water transport in the surrounding sediments (termed bioirrigation) depend upon sediment permeability. Sandy sediment typically possesses high enough permeability to allow advective flow of pore water through the interconnected pore space surrounding sediment particles. Under these conditions, the pressure head within a burrow created by burrow ventilation activities can drive pore-water flow from the burrow into surrounding sediments. The velocity of this flow can be calculated using Darcy s law: u d ¼ k ðrp rgrxþ m ½3Š where u d is the Darcy velocity, k is sediment permeability, m is the dynamic viscosity of pore water, P is pressure, r is the pore-water density, g is gravity, and r is a gradient The velocity of pore water, u, is related to the Darcy velocity, u d ¼ uj 1, where j ¼ porosity. Substituting eqn [3] into the general diagenetic equation gives the expected change in concentration of a pore-water tracer subjected to an advection velocity driven by burrow ventilation, molecular diffusion, and chemical 2 C D þ X R; xol ½4Š where D M is the molecular diffusion coefficient, corrected for tortuousity. In contrast to sandy sediments, permeability of mud is generally too low to permit significant porewater advection so that u ¼. Thus, pore-water transport in muddy sediments is dominated by molecular diffusion. Burrow ventilation in muddy sediments enhances pore-water transport by changing the diffusive geometry. Figure 3 shows the geometry of idealized equally spaced vertical
5 BIOTURBATION 399 (a) (b) (c) r x Figure 3 Idealized burrow geometry underlying eqn [5]. (a) Burrows as close-packed cylinders. (b) Rectangular plane intersecting an average burrow microenvironment. (c) The x r domain of eqn [5]. The shaded rectangle represents the burrow, while the unshaded rectangle represents the surrounding sediment. Reproduced from Aller RC (198) Quantifying solute distributions in the bioturbated zone of marine sediments by defining an average microenvironment. Geochimica et Cosmochimica Acta 44(12): , with permission from Elsevier. burrows embedded into sediment. If these burrows were rapidly flushed so that the solute concentration within the burrows were equal to the solute concentration in the overlying water, then the corresponding diagenetic equation governing pore-water transport in the vertical dimension, x, and in the radial dimension, r, would be given ¼ D 2 2 þ þ X R The diffusion operator within the parentheses is similar to the diffusion operator in eqn [4], but quantifies molecular diffusion in both the x and r dimensions. A one-dimensional diagenetic model that incorporates the effects of bioirrigation on porewater transport can be derived from eqn 2 C D 2 aðc C Þþ X R ½6Š where a(day 1 ) is the coefficient of nonlocal bioirrigation, and C is the concentration of the solute tracer in overlying water. The nonlocal bioirrigation coefficient, a, in eqn [6] treats bioirrigation as both a source and a sink for solutes at depth. The value of the bioirrigation exchange rate, a, is usually determined by measuring dissolved porewater tracers with known inputs and reaction kinetics. The most commonly used radionuclide tracer of bioirrigation is 222 Rn. Produced within sediments from the decay of its parent 226 Ra, 222 Rn is a soluble noble gas. Pore-water exchange with overlying water results in lower 222 Rn activity in sediment pore waters than would be expected, compared to the activity of its parent 226 Ra. The shape of the 222 Rn profile and the magnitude of the 222 Rn deficit relative to 226 Ra are used to determine rates of bioirrigation ½5Š Depth (cm) 222 Rn activity (dpm ml 1 ) Measured 222 Rn activity Supported 222 Rn activity Nonlocal model solution Figure 4 Measured 222 Rn activity and supported 222 Rn activity (produced from the decay of 226 Ra within sediment particles) vs. depth in a sediment core from Boston Harbor, Massachusetts. Horizontal error bars represent standard error from three replicate cores. The bioirrigation rate, a (day 1 ), was modeled as the exponential function. a ¼ 3.8e x, and the modeled profile was calculated from eqn [6]. Data from Shull DH, previously unpublished. (Figure 4). Other tracers of pore-water exchange include inert solutes such as bromide or dissolved nutrients such as ammonium, nitrate, or silicate, if reaction kinetics can be estimated. Bioirrigation has important implications for sediment geochemistry. Bioirrigation accelerates sediment water fluxes, changes rates of elemental cycling, catalyzes oxidation reactions in the sediment, changes vertical and horizontal gradients of pore-water solutes, elevates levels of dissolved oxygen, and reduces
6 4 BIOTURBATION exposure of organisms to metabolic wastes. By changing the redox geometry of sediments, bioirrigation can significantly alter rates of redox-sensitive reactions that occur in sediments such as nitrification, denitrification, sulfate reduction, and mercury methylation. Bioturbation and the Ecology and Evolution of Benthic Communities Bioturbation has numerous effects on benthic community structure. In muddy sediments, bioturbation by deposit feeders appears to reduce densities of suspension feeders. Conveyor-belt bioturbation can displace surface-dwelling benthos. Bioturbation changes the depth distribution of organic matter and can increase the inventory and quality of food for deposit feeders in sediments. It can increase nutrient fluxes leading to elevated rates of benthic primary production and increased microbial productivity as well. Furthermore, elevated nutrient recycling between sediments and overlying water helps to maintain water-column productivity in estuaries and other shallow-water marine environments. Marine benthic habitats of the late Neoproterozoic and early Phanerozoic (6 5 Ma) were very different from benthic habitats that existed later. Seafloors at this time were characterized by welldeveloped microbial mats, as suggested by studies of sedimentary fabric preserved in the geologic record. These extensive microbial mats and associated seafloor fauna, such as immobile suspension-feeding helicopacoid echinoderms, became scarce or extinct in the Cambrian. The substantial change that occurred in seafloor communities around this time, termed the Cambrian substrate revolution, is thought to be caused by the development of bioturbation. It is hypothesized that the emergence of both bioturbation and predation around this time led to the extinction of nonburrowing taxa and influenced subsequent development of animal body plans during the Cambrian. Bioturbation also made a new food resource, buried organic matter, accessible to deposit feeders while radically changing the geochemistry of the seafloor. See also Macrobenthos. Ocean Margin Sediments. Sediment Chronologies. Sedimentary Record, Reconstruction of Productivity from the. Uranium-Thorium Decay Series in the Oceans Overview. Uranium-Thorium Series Isotopes in Ocean Profiles. Further Reading Aller RC (198) Quantifying solute distributions in the bioturbated zone of marine sediments by defining an average microenvironment. Geochimica et Cosmochimica Acta 44(12): Aller RC (1982) The effects of macrobenthos on chemical properties of marine sediments and overlying waters. In: McCall PL and Tevesz MJS (eds.) Animal Sediment Relations, pp New York: Plenum. Boudreau BP and Jorgensen BB (21) The Benthic Boundary Layer: Transport Processes and Biogeochemistry. Oxford, UK: Oxford University Press. Dorgan KM, Jumars PA, Johnson BD, Boudreau BP, and Landis E (25) Burrowing by crack propagation: Efficient locomotion through muddy sediments. Nature 433: 475. Lohrer AM, Thrush SF, and Gibbs MM (24) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431: Meysman F, Boudreau BP, and Middelburg JJ (23) Relations between local, non-local, discrete and continuous models of bioturbation. Journal of Marine Research 61: Shull DH (21) Transition-matrix model of bioturbation and radionuclide diagenesis. Limnology and Oceanography 46(4):
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