BIOTURBATION

D. H. Shull, Western Washington University, individual organisms increase with increasing body Bellingham, WA, USA size so that bioturbation rates in some sedimentary & 2009 Elsevier Ltd. All rights reserved. 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 Introduction into the following categories: conveyor-belt feeding where particles are collected at depth and deposited Activities of organisms inhabiting seafloor sediments at the sediment surface; subductive feeding, where (termed benthic infauna) are concealed from visual particles are collected at or near the sediment surface observation but their effects on sediment chemical and and deposited at depth; and interior feeding where physical properties are nevertheless apparent. Sedi- particles are collected and deposited within the ment ingestion, the construction of pits, mounds, fecal sediment column. These feeding modes transport pellets, and burrows, and the ventilation of subsurface particles the length of the organism’s body or the burrows with overlying water significantly alter rates length of its burrow. Some species of deposit feeders of chemical reactions and sediment–water exchange, also ingest and egest sediment near the sediment destroy signals of stratigraphic tracers, bury reactive surface, resulting in horizontal movement of par- organic matter, exhume buried chemical contami- ticles but limited vertical displacement. Due to rapid nants, and change sediment physical properties such particle ingestion rates and relatively large horizontal as grain size, porosity, and permeability. Biogenic and vertical transport distances, deposit feeding is sediment reworking resulting in a detectable change in considered to be the primary agent of bioturbation. sediment physical and chemical properties is termed Benthic organisms also rework sediments through bioturbation. It is critical to account for bioturbation burrow formation. Muddy sediments behave more when calculating chemical fluxes at the sediment– like elastic solids than granular material. A benthic water interface and when interpreting chemical pro- burrower in muddy sediments uses its burrowing files in sediments. In the narrowest sense, bioturbation apparatus (bivalve foot, polychaete proboscis, am- refers to the biogenic transport of particles that des- phipod carapace, or other burrowing tool) like a troys stratigraphic signals. In the broader sense it can wedge to create and propagate cracks in sediments. refer to biogenic transport of pore water and changes After an organism passes through a crack, sediments in sediment physical properties due to organism tend to rebound viscoelastically resulting in relatively activities as well. Bioturbation and its effects on sedi- little net movement of particles compared to deposit ment chemistry and stratigraphy is a natural con- feeding. An exception to this generality is burrowing sequence of adaptation by organisms to living and by large epibenthic predators including skates, rays, foraging in sediments. and benthic-feeding marine mammals such as gray whales and walrus, which can cause extensive re- Particle Bioturbation working in sediment patches where they are feeding. From a particle’s perspective, bioturbation consists Deposit feeding, the ingestion of particles comprising of relatively short-lived intervals of particle move- sedimentary deposits, is the dominant feeding strat- ment due to deposit feeding or burrowing inter- egy in muddy sediments. In fact, since the vast ma- spersed by relatively long periods during which the jority of the ocean is underlain by muddy sediments, particles remain at rest. When particles pass through deposit feeding is the dominant feeding strategy on animal guts, in addition to changing location, the the majority of the Earth’s surface. Because digestible particles may be aggregated into fecal pellets (par- organic matter typically comprises less than 1% of ticles surrounded by or embedded in mucopolymers). sediments by mass, to meet their metabolic needs When constructing burrows, some infauna produce deposit feeders exhibit rapid sediment ingestion mucopolymer glue to form sturdy burrow walls, rates, averaging roughly three body weights per day. locking particles into place for an extended period of Deposit feeders adapted to living in sediments with time. Transport of subsurface particles to the sedi- relatively low organic matter concentrations tend to ment surface by conveyor-belt feeding results in exhibit elevated ingestion rates; there is no free lunch downward gravitative movement of particles within even for deposit feeders. Rates of deposit feeding of the sediment column as subsurface feeding voids are

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filled with sediment from above. Within a particular remember rule of thumb regarding bioturbation rates 2 1 sedimentary habitat many particle reworking mech- is that DB varies from c. 0.01 to 100 cm yr from anisms occur simultaneously. deep-sea to shallow-water depths. This variation is There are many ways to quantify mathematically correlated with increased abundance of infauna, the ensemble of particle motions that results in greater rates of food supply, and (with the exception bioturbation. Traditionally, bioturbation has been of polar regions) elevated average bottom-water modeled as though it were analogous to diffusion. temperatures with decreasing water depth. This means that the collection of particle motions Because bioturbation mechanisms can transport resembles a large number of small random dis- particles relatively large distances, roughly the length placements. Under these assumptions, bioturbation of the reworked zone, L, and because particle tra- is included in the general diagenetic equation as a jectories are often nonrandom, the biodiffusion co- biodiffusion coefficient, DB. Ignoring vertical gradi- efficient is not appropriate for modeling the effects of ents in porosity and sediment compaction, the rate of bioturbation on transport of some tracers. A more change of a chemical tracer, C, in the vertical spatial general model of particle mixing that includes dimension, x, can be represented as follows: longer-distance, nonrandom particle trajectories is the nonlocal bioturbation model. Again neglecting @C @2C @C X variation in porosity: ¼ DB u þ R; xoL ½1 @t @x2 @x ZL where D is the biodiffusion coefficient (cm2 yr 1), B @C 0 0 1 ¼ Kðx ; x; tÞCðx Þdx Pu is the sediment accumulation rate (cm yr ), and @t R represents the sum of chemical reactions. In the 0 absence of specific information on bioturbation ZL X 0 0 @C mechanisms, it is often assumed that DB is constant CðxÞ Kðx; x ; tÞdx u þ R ½2 throughout the reworked layer to the depth L. Below @x 0 the depth L, DB is zero. The advantage of this formulation is that all the various particle reworking where K is the exchange function (dimensions: processes are quantified by one parameter, DB. time 1) that quantifies the rate of particle movement 1 The nondimensional Peclet number, Pe ¼ uLDB , from one depth, x, to any other depth, x0. The first quantifies the relative importance of bioturbation term on the right-hand side gives the concentration and sediment accumulation in determining the pro- change at depth x due to the delivery of a particle file of C within the reworked layer. Values of Pe less tracer from other depths, x0. The second term gives than 1 indicate a strong influence of bioturbation. the concentration change at depth x due to transport Table 1 summarizes the general pattern of variation of a tracer from depth x to other depths x0. The other in DB, u, L, and Pe among benthic provinces at terms are defined as in eqn [1]. The exchange func- different water depths. The depth of the reworked tion, K, can potentially quantify a complex ensemble layer, L, shows little systematic variation among of bioturbation mechanisms. Analogs of eqn [2] that habitats, averaging 10 cm. Although we would ex- rely on discrete mathematics exist. In one dimension, pect considerable variation in Pe, the low values in nonlocal transport can be modeled as a transition each province indicate that bioturbation is generally matrix in which the rows of the transition matrix important throughout the ocean. An easy-to- correspond to depths in the sediment and the matrix elements quantify the probability of transport of a tracer among depths. Multiple-dimensional au- Table 1 Variation in the biodiffusion coefficient, DB, sedimen- tomaton models can simulate complex modes of tation rate, u, and the Peclet number, Pe, characteristic of different benthic environments. A Peclet number greater than 1 particle transport in both vertical and horizontal indicates sediment accumulation is more important than dimensions. These more complex models can better bioturbation capture the complexities of bioturbation but sacrifice the one-parameter simplicity of eqn [1]. DB uLPe There are two common approaches for determining

Shallow water 10 100 0.1 1 10 0.01 1 the values of the bioturbation parameters in these Cont. Shelf 0.1 10 0.01 0.5 10 0.01 50 models. Mixing parameters can be estimated from Slope 0.05 1 0.001 0.05 10 0.01 10 direct measurements of deposit-feeder ingestion rates Deep sea 0.01 0.5 0.0001 0.01 10 0.002 10 and organism burrowing rates. More often, these A Peclet number less than 1 indicates that bioturbation is more parameters are estimated by measuring sediment- important for transport relative to sedimentation. bound tracers with known inputs to the sediment and BIOTURBATION 397

P known reaction rates ( R). Mixing parameters are Bioturbation makes it generally difficult or im- then calculated by fitting measured tracer profiles to possible to resolve timescales of less than 103 years profiles calculated by use of the appropriate math- stratigraphically in deep-sea sediment cores. If the ematical model. Useful bioturbation tracers include bioturbation mechanism is not known, it is difficult excess activities of naturally occurring particle- to separate changes in the input signal from changes reactive radionuclides such as 234Th, 210Pb, or 7Be. due to mixing (Figure 2). If mixing is not complete, These radionuclides have a relatively continuous and the bioturbation mechanism is known, it may be source either from the atmosphere or from the over- possible to deconvolve the input signal to the strati- lying water column, are rapidly scavenged onto par- graphic record, although detailed information will be ticles, and sink to the seafloor (see Sediment lost. If bioturbation in the surface reworked zone Chronologies). In addition, chlorophyll a,artificial completely homogenizes a tracer, then knowing the tracers added to the sediment surface as an impulse mixing mechanism is unimportant. Once pancake such as glass beads or fluorescent luminophores, or batter is thoroughly mixed, for example, it no longer other exotic identifiable material with a known rate of contains information on how the mixing was input are used as tracers of bioturbation. The profile performed. of excess 210Pb in Figure 1 illustrates several effects Bioturbation has important consequences for of bioturbation on a tracer profile. The rate of sediment geochemistry. Bioturbation buries reactive bioturbation in the top 6 cm is rapid enough to organic matter. Subductive deposit feeders selectively completely mix excess 210Pb within this layer. The feed on organic-rich particles near the sediment sur- subsurface peak at 15–16 cm indicates subsurface face and deposit them at depth, perhaps as food deposition of surficial material. Below 16 cm, the caches. In the presence of horizontal transport of slope of the profile is set by the rate of sediment ac- organic matter, or suspension-feeding benthos that cumulation and radioactive decay of 210Pb. locally enhance organic matter deposition through Bioturbation has important consequences for biodeposit formation, bioturbation can greatly sediment stratigraphy, chemistry, and biology. Bio- enhance the organic matter inventory in sediments. turbation can homogenize tracers within the re- Burial of organic matter exposes it to different worked layer (Figure 1). Bioturbation acts as a oxidants, changing the degradation pathway. In low-pass filter, destroying information deposited on particular, reworking of Mn and Fe oxides cycles short timescales, but preserving longer-term trends. them between oxidative and reducing environments,

210 −1 Excess Pb (dpm g ) Tracer concentration 0 5 10 15 0 0.2 0.4 0.6 0.8 1 0 0 Well-mixed surface layer 5 5

10 10

Subduction of 15 surficial 210Pb 15 Depth (cm) Depth (cm) 20 20 Sediment accumulation below reworked layer 25 25

30 30 Figure 1 Excess 210Pb activity vs. depth in a sediment core from Narragansett Bay, Rhode Island. Data with permission from Figure 2 Changes in the profile of a hypothetical conservative Shull DH (2001) Transition-matrix model of bioturbation and tracer present initially as two narrow subsurface peaks, as 2 1 1 radionuclide diagenesis. Limnology and Oceanography 46(4): predicted from eqn [1]. DB ¼ 0.1 cm yr , u ¼ 0.1 cm yr , 905–916. Copyright (2001) by the American Society of Limnology L ¼ 10 cm. Solid line: tracer profile at t ¼ 0. Dotted line: and Oceanography, Inc. t ¼ 25 years. Dashed line: t ¼ 150 years. 398 BIOTURBATION resulting in enhanced anaerobic degradation of or- surface sediments generally contain more pore water ganic matter. than particles. The rate of molecular diffusion of Bioturbation changes sediment properties as well. solutes through pore water is reduced relative to Pelletization changes the sediment grain size distri- diffusion in a free solution because the solutes must bution. Furthermore, bioturbation rates are particle- follow a winding path through the particles, called size-dependent. Size-selective feeding by deposit sediment tortuousity. Particle bioturbation mech- feeders results in biogenic graded bedding with lag anisms redistribute this pore water along with the layers of large sediment particles either at the sedi- particles, but since rates of pore-water transport, ment surface or at depth, depending upon the bio- inferred from dissolved tracer distributions, are turbation mechanism. Formation of pellets and typically an order of magnitude higher than rates of burrows increases sediment porosity, counteracting particle bioturbation, particle reworking is a rela- the effects of sediment compaction. Sediment surface tively unimportant mechanism for transporting pore manifestations of bioturbation such as pits, mounds, water. Rather, burrow ventilation seems to be the and tubes alter seafloor roughness and flow charac- most important biogenic mechanism of pore-water teristics of the benthic boundary layer, roughly transport. The consequences of burrow ventilation doubling the drag compared to a hydrodynamically on pore-water transport in the surrounding sedi- smooth bed. ments (termed bioirrigation) depend upon sediment permeability. Sandy sediment typically possesses high enough Pore-Water Bioirrigation permeability to allow advective flow of pore water through the interconnected pore space surrounding Most benthic infauna maintain a burrow that con- sediment particles. Under these conditions, the nects to the sediment–water interface to facilitate pressure head within a burrow created by burrow respiration, feeding, defecation, and other metabolic ventilation activities can drive pore-water flow from processes. These burrows exist in a range of geom- the burrow into surrounding sediments. The velocity etries including vertical cylinders, U-orJ-shaped of this flow can be calculated using Darcy’s law: tubes, or branching networks. In deep-sea sediments, dissolved oxygen can penetrate 30 m into the sedi- k u ¼ðrP rgrxÞ½3 ment. Near the shore, however, oxygen penetration d m is quite variable and in muddy sediments it often penetrates no farther than a few millimeters. To meet where ud is the Darcy velocity, k is sediment per- their metabolic requirements for oxygen, infauna meability, m is the dynamic viscosity of pore water, P ventilate their burrows by thrashing their bodies, is pressure, r is the pore-water density, g is gravity, flapping their appendages, by peristalsis, by beating and r is a gradient operator (e.g., @/@x, @/@y). The cilia, or by oscillating like pistons in their tubes. velocity of pore water, u, is related to the Darcy 1 These ventilation mechanisms result in intermittent velocity, ud ¼ uj , where j ¼ porosity. Substituting burrow flushing, which exchanges a portion of the eqn [3] into the general diagenetic equation gives the fluid inside the burrow with overlying water. In this expected change in concentration of a pore-water way, organisms in the sediment can flush out meta- tracer subjected to an advection velocity driven by bolic wastes and toxins such as hydrogen sulfide that burrow ventilation, molecular diffusion, and chem- have accumulated in their burrows and they can re- ical reactions: stock the burrow water with dissolved oxygen. Ob- servations of organisms in artificial tubes maintained @C @2C @C X ¼ D0 u þ R; xoL ½4 in the laboratory indicate that burrow ventilation is @t M @x2 @x episodic, with ventilation frequencies ranging from 0 once per hour to 10 or more ventilation events per where D M is the molecular diffusion coefficient, hour. Deposit-feeding infauna generally ventilate less corrected for tortuousity. frequently than suspension-feeding infauna, which In contrast to sandy sediments, permeability of pump water through their burrows for both respir- mud is generally too low to permit significant pore- ation and food capture. water advection so that u ¼ 0. Thus, pore-water The sediments into which these burrows are built transport in muddy sediments is dominated by mo- are mixtures of particles and interconnected pore lecular diffusion. Burrow ventilation in muddy water. Surficial sediments may possess porosities sediments enhances pore-water transport by chan- (defined as the volume of interconnected pore water ging the diffusive geometry. Figure 3 shows the per unit volume of sediment) in excess of 90%. Thus, geometry of idealized equally spaced vertical 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 (1980) Quantifying solute distributions in the bioturbated zone of marine sediments by defining an average microenvironment. Geochimica et Cosmochimica Acta 44(12): 1955–1965, with permission from Elsevier. burrows embedded into sediment. If these burrows 222 −1 were rapidly flushed so that the solute concentration Rn activity (dpm ml ) within the burrows were equal to the solute con- 0 0.05 0.1 0.15 0.2 0.25 0 centration in the overlying water, then the corres- ponding diagenetic equation governing pore-water transport in the vertical dimension, x, and in the 5 radial dimension, r, would be given by 2 X @C 0 @ C 1 @ @C ¼ D þ r þ R ½5 10 @t M @x2 r @r @r

The diffusion operator within the parentheses is similar to the diffusion operator in eqn [4], but Depth (cm) 15 quantifies molecular diffusion in both the x and r Measured 222Rn activity dimensions. A one-dimensional diagenetic model that incorporates the effects of bioirrigation on pore- 20 Supported 222Rn activity water transport can be derived from eqn [5]: Nonlocal model solution 2 X @C @ C 25 ¼ D0 aðC C Þþ R ½6 @t M @x2 0 Figure 4 Measured 222Rn activity and supported 222Rn activity where a(day 1) is the coefficient of nonlocal bioir- (produced from the decay of 226Ra within sediment particles) vs. depth in a sediment core from Boston Harbor, Massachusetts. rigation, and C0 is the concentration of the solute tracer in overlying water. The nonlocal bioirrigation Horizontal error bars represent standard error from three replicate cores. The bioirrigation rate, a (day 1), was modeled coefficient, a, in eqn [6] treats bioirrigation as both a as the exponential function. a ¼ 3.8e x, and the modeled profile source and a sink for solutes at depth. was calculated from eqn [6]. Data from Shull DH, previously The value of the bioirrigation exchange rate, a,is unpublished. usually determined by measuring dissolved pore- water tracers with known inputs and reaction kin- (Figure 4). Other tracers of pore-water exchange etics. The most commonly used radionuclide tracer include inert solutes such as bromide or dissolved of bioirrigation is 222Rn. Produced within sediments nutrients such as ammonium, nitrate, or silicate, if from the decay of its parent 226Ra, 222Rn is a soluble reaction kinetics can be estimated. noble gas. Pore-water exchange with overlying water Bioirrigation has important implications for sedi- results in lower 222Rn activity in sediment pore ment geochemistry. Bioirrigation accelerates sediment– waters than would be expected, compared to the water fluxes, changes rates of elemental cycling, activity of its parent 226Ra. The shape of the 222Rn catalyzes oxidation reactions in the sediment, changes profile and the magnitude of the 222Rn deficit relative vertical and horizontal gradients of pore-water solutes, to 226Ra are used to determine rates of bioirrigation elevates levels of dissolved oxygen, and reduces 400 BIOTURBATION exposure of organisms to metabolic wastes. By chan- influenced subsequent development of animal body ging the redox geometry of sediments, bioirrigation plans during the Cambrian. Bioturbation also made a can significantly alter rates of redox-sensitive reactions new food resource, buried organic matter, accessible that occur in sediments such as nitrification, denitrifi- to deposit feeders while radically changing the geo- cation, sulfate reduction, and mercury methylation. chemistry of the seafloor.

Bioturbation and the Ecology and See also Evolution of Benthic Communities Macrobenthos. Ocean Margin Sediments. Sediment Bioturbation has numerous effects on benthic com- Chronologies. Sedimentary Record, Reconstruction munity structure. In muddy sediments, bioturbation of Productivity from the. Uranium-Thorium Decay by deposit feeders appears to reduce densities of Series in the Oceans Overview. Uranium-Thorium suspension feeders. Conveyor-belt bioturbation can Series Isotopes in Ocean Profiles. displace surface-dwelling benthos. Bioturbation changes the depth distribution of organic matter and Further Reading can increase the inventory and quality of food for deposit feeders in sediments. It can increase nutrient Aller RC (1980) Quantifying solute distributions in the fluxes leading to elevated rates of benthic primary bioturbated zone of marine sediments by defining an production and increased microbial productivity as average microenvironment. Geochimica et Cosmochi- well. Furthermore, elevated nutrient recycling be- mica Acta 44(12): 1955--1965. tween sediments and overlying water helps to Aller RC (1982) The effects of macrobenthos on chemical maintain water-column productivity in estuaries and properties of marine sediments and overlying waters. In: McCall PL and Tevesz MJS (eds.) Animal–Sediment other shallow-water marine environments. Relations, pp. 53--102. New York: Plenum. Marine benthic habitats of the late Neoproter- Boudreau BP and Jorgensen BB (2001) The Benthic ozoic and early Phanerozoic (600–500 Ma) were very Boundary Layer: Transport Processes and Biogeo- different from benthic habitats that existed later. chemistry. Oxford, UK: Oxford University Press. Seafloors at this time were characterized by well- Dorgan KM, Jumars PA, Johnson BD, Boudreau BP, and developed microbial mats, as suggested by studies of Landis E (2005) Burrowing by crack propagation: sedimentary fabric preserved in the geologic record. Efficient locomotion through muddy sediments. Nature These extensive microbial mats and associated sea- 433: 475. floor fauna, such as immobile suspension-feeding Lohrer AM, Thrush SF, and Gibbs MM (2004) Bioturbators helicopacoid echinoderms, became scarce or extinct enhance ecosystem function through complex biogeo- in the Cambrian. The substantial change that oc- chemical interactions. Nature 431: 1092--1095. Meysman F, Boudreau BP, and Middelburg JJ (2003) curred in seafloor communities around this time, Relations between local, non-local, discrete and termed the ‘Cambrian substrate revolution’, is continuous models of bioturbation. Journal of Marine thought to be caused by the development of bio- Research 61: 391--410. turbation. It is hypothesized that the emergence of Shull DH (2001) Transition-matrix model of bioturbation both bioturbation and predation around this time and radionuclide diagenesis. Limnology and Oceano- led to the extinction of nonburrowing taxa and graphy 46(4): 905--916.