Bioturbation: A Facilitator of Contaminant Transport in Bed Sediment

Weldon S. Bosworth
Balsam Environmental Consultants, Inc., 5 Industrial Way, Salem, NH 03079 and

Louis J. Thibodeaux
Hazardous Waste Research Center, Louisiana State University, Baton Rouge, LA 70803-6421 The biological activity o f benthic organism (=bioturbation)in bed sediments can be signifiantly more important thun physicochemical processes in the movement of sediment particles and interstitial constituents within the sediment column and to the overlying water. Bioturbationf magnitude more rapid driven transport processes may be several orders o than molecular-driven processes for some constituents, i.e., particle reactive compounds like PCB, when considered on a chemical pore water concentrationgrcrdierrtbash. Benthic organism aflect particle redistribution and solute transport by burrowing, ingestionlexcretion, tubebuilding and biodqosition. In most benthic environments, whether freshwater, estuarine or marine, numbers of organisms and rates o f sediment turnover are highest in the oxygenated zone above the redox boundary, generally the top 2-5 cm of the sediment column. However,a variety o f organisms penetrate deeper into the sediment and may also be important in transport of both dissolved and particle reactive constituents. W h e n considering capping of contaminated sediment in pluce or capping of contaminated dredge spoils, the ejJects of bioturbaticm on the mobility of the contaminants must first be considered before establishing engineering design criteria. Capping of contaminated bed sediments or dredge spoils can e h a t e the bioturbated zone above the contaminated bed sediment and thus potentially reduce the rate of contaminant transport by several orders o f magnitude.
INTRODUCTION

It is well known that bottom dwelling organisms in both marine and fresh water environments are capable of substantially altering the biological, physical and chemical properties of the bottom sediment. Their activities, including ingestion and excretion, burrowing, tube building and biodeposition, can substantially modify sediment stability and erodibility, vertical distribution of dissolved and particulate materials within the sediment, the transport of material within the sediment and across the sediment water interface as well as affect the presence and abundance of other species in the benthic community. The purpose of this review is to examine how bioturbation may affect the transport of contaminants within the bed sediment and across the sediment water interface. A review of the characteristics of bioturbation, including species involved, depths of bioturbation, as well as how bioturbation can affect both physical and chemical properties of the sediment is first presented. We then present
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an example of how bioturbation may facilitate contaminant transport and why bioturbation must be taken into consideration in developing engineering design criteria for remediation of contaminated bed sediment in fresh water, estuarine and marine environments. A framework for developing site-specific information on the effect of bioturbation is also discussed.
BIOTURBATION: ACTIVITIES OF BENTHIC ORGANISMS

Benthic organisms are generally divided into groups based on life mode and niche. Epifauna are those benthic species that live temporarily or permanently on the sediment surface. They are generally mobile and include invertebrate species such as crabs, lobster, and snails as well as vertebrate species such as bottom-living fish, e.g., skates, rays and flatfish. For purposes of discussing bioturbation, birds such as geese and wading birds could also be considered epifauna. Species living within the sediment, whether they feed within the sediment or from
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..........,.

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Figure 3. Vertical distribution of infauna in sand and mud. After Hines and Comtois (1 985).

Figure 1. Feeding types of benthic organisms. After Rhoads (1974).

that live within the sediment. A special group of subsurface feeders is formed by conveyor-belt feeders [ I ] which are oriented head down, pumping subsurface reduced sediments through their bodies and depositing them on the sediment surface. Demersal or bottom-living fish generally feed at or near the sediment surface, often actively disturbing the sediment while foraging for infaunal organisms [ 2 , 3 ] . Birds can also be important bioturbators, shallow wading birds probing into the sediment bed for their prey [a] or other dabbling or paddling species which move the sediment in order to float their prey to the sediment surface where Some bird species are herbivorous and feed they eat it [q. on rhizomes of various aquatic grasses thereby disturbing the sediment [S].
DEPTHS OF BIOTURBATION

the overlying water, are termed infauna. These infaunal organisms range from small meiofauna to larger macrofauna like polychaetes, crustaceans, and molluscs. Infaunal organisms are generally categorized into two groups based on their feeding mode: surface feeders are those species which feed at the sediment-water interface or from the overlying water column, and subsurface feeders which feed below the sediment water interface (Figure 1).Surface feeders include suspension feeders which siphon water from the overlying water column, surface deposit feeders which obtain their food from the surface of the sediment and a group of organisms which transport sediment from the surface passing it through their bodies and depositing it again on the surface. Subsurface feeders include deposit feeding species which may process sediment through their bodies and those which burrow through the sediment bed feeding on the detrital deposits within the sediments or organisms

Benthic scientists studying niche diversity or ecology of benthic communities as well as physical and chemical dynamics of the sediment bed have documented the vertical distribution of infaunal organisms in many different types of sediments and environments [ I , 3, 7-17]. Typically, vertical stratification of infaunal species reflects or is related to differences in burrowing abilities, body size, lifestyle and environmental conditions [18].Burrowing
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depths can also be affected by a variety of biotic and abiotic factors. Seasonality, interspecific competition, and predation [19], as well as environmental factors, can affect the vertical distribution of species. Organisms in physically disturbed or pollutant-impacted environments are often limited to the upper few centimeters of sediment; whereas, in less physically impacted or less polluted environments, organisms tend to be found at deeper depths within the sediment (Figure 2) [20,21].Sediment character can also influence the nature of the species that colonize the sediments and thus indirectly affect the depth of bioturbation in those environments. Hines and Comtois [17],for instance, noted a slightly greater depth penetration in muddy sediments than in sandy sediments (Figure 3). The general pattern for infaunal distribution, whether in fresh water (Figure 4), estuarine or marine environments, is that the greatest numbers of organisms occur within 2 to 5 centimeters of the sediment surface, with very few numbers of organisms being found deeper than 20 cm. Since larger species (e.g., bivalves, polychaete worms and burrowing shrimps) tend to live deeper within the sediment, distribution of benthic biomass tends to be deeper with the greatest fraction occurring below 5 cm in healthy undisturbed environments. Large bivalves (e.g., Mya arenaria [17] and Ensis directus [22]),as well as some polychaete worms E23, 24, 251 and burrowing

shrimp (e.g., Squilla empusa), have the ability to burrow deeper than 20cm and some may be found as deep as 60 cm [26].Indeed, Myers [26] reported that winter burrows of the mantis shrimp, s. empusa, can reach as deep as four meters.

EFFECTS OF BIOTURBATION O N PHYSICAL AND CHEMICAL PROPERTIES OF SEDIMENT

The effect of bioturbation on sediment stratigraphy has been documented by many authors [9,21,27-311.These studies document mixing to a depth of 3 to 20 cm with little disturbance below 20 cm. Bioturbation can biologically mediate changes in those sedimentary properties which are important for determining sediment stability. These changes include increase of sediment bed roughness, increase in grain size through the formation of fecal pellets and secretion of mucopolysaccharides and changes in sediment packing, sheer strength and water content [21]. Bed roughness can result from burrowing and foraging activity, construction of tubes which project above the sediment surface as well as the production of dense concentrations of shell material at the sediment water interNovember, 1990

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face. Depending on the magnitude of these bioturbation phenomena, sediments may be stabilized as in the case of substantial tube fields or destabilized as in the case of the development of considerable sediment bed topography through burrowing and mounding by infaunal species. While feeding by benthic species often involves shredding and tearing of the detrital materials and can result in a decrease in mean size of particulate organic matter, the transformation of detrital material and fine sediments into larger size fecal pellets can increase the porosity of the sediment. This increase in porosity can lead to an increase in water content and a decrease in sheer strength of the sediment bed. However, mucopolysaccharides as well as mucous produced by microbial and meiofaunal species feeding on fecal pellets can increase the binding strength of the sediment bed and lead to increases in critical entrainment velocities by as much as 60 percent [ Z l ] . In a similar manner geotechnical properties such as density, water content and sheer strength are all influenced substantially by benthic organisms. The overall effect depends upon the nature of the sedimentand the rate of bioturbation activity as well as seasonal factors. The distribution of many geotechnical properties with depth is highly correlated with the presence and activities of bioturbating species. For example, a study of the Rhoads [I] found that the water content of the sediment was higher in the shallower depths, the zone of more active bioturbation. Likewise, Myers [9]found that sediment compactness was substantially decreased in the upper few cm of the sediment column (Figure 5). Bioturbation can also influence the chemical properties of the sediment bed in a variety of ways. Aller [32] indicated that the hypothetical. biogeochemical reaction distribution could be affected by . . . 1. material is translocated continuously between reaction zones. during feeding, burrowing and tube construction, 2. burrow and fecal pellet formation alters reaction and solute diilusion geometries, creating a mosaic of biogeochemical microenvironments rather than a vertically stratified distribution, 3. new reactive organic substrates in the form of mucus secretions may be introduced into the deposit independent of sedimentation processes, 4. feeding and mechanical disturbance may influence the microbial pop

ulations that mediate reactions, 5. sedimentary materials may also be directly altered during passage of the material through the organisms guts. The most basic effect of bioturbation is the nonselective or homogeneous mixing of sediment during feeding, burrowing and tube building activities. The sediment particles are biologically transported at a different rate or in a different way than either net sediment deposition or than would be predicted from chemical diffusion processes in the sediment. Some species are capable of selecting particles on the basis of particle position in the sediment, size, shape, surface texture and density. This selection may result in segregation of different classes of particles as well as related chemical properties of the sediment [21]. The movement of solutes can also be greatly affected by bioturbation. While movement of solutes in the absence of bioturbation is controlled by molecular diffusion and advection, movement of infaunal species as well as construction and irrigation of burrows can substantially change characteristics of solute transport. Typically, increased apparent diffusion coefficients of solutes when affected by bioturbation can be 10 to 1000 times higher than sediment molecular diffusion coefficients for the same deposits in the absence of bioturbation [32,33]. The feeding and respiration of infauna can also result in advection of surrounding pore waters, particularly in more permeable sands. Some species may even use permeable sediments as a filter for respiratory currents to augment food supply either by capture of suspended material or by stimulating local populations of bacteria [32]. Many tubes, however, are lined by polysaccharide membranes which are permeable to diffusive transport of solutes but not to advective flow [32]. Because of the relatively impermeable nature of the muddy sediments toward advective flow, the advection of pore water in these environments is probably due more to the movement of mobile benthos or periodic collapse of burrow walls [32]. The irrigation of tubes by some species and the burrowing activities of other species may increase the penetration of the aerobic zone into the sediment. Rhoads [34]

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observed that both the quantity and quality of colonizing species affected the process of sediment oxygenation in some areas. Where deep burrowing deposit feeders were found at high densities, major changes in the sediment redox potential discontinuities were observed. In some cases the redox layer was depressed 2 to 3 cm by particle reworking and irrigation of deeper feeding infauna. Since tubes effectively increase the area of sedimenvwater interface, burrows of some deeper burrowing species can extend the depth of the oxidized zone and even create oxidized microenvironments within the anaerobic zone [35l. Bioturbation has also been reported to cause substantial effects on hydrogen and phosphorus dynamics as well on the distribution of sediment constituents [32, 351. The distribution of a number of sediment chemical constituents with depth are highly correlated with the activities of bioturbating species and presence of tubes. For example, McCaffrey et al. [38]and Riedel et al. [37l reported differences in vertical distribution of sediment chemical parameters that they related to the activity of benthic organisms.
BIOTURBATION AND CONTAMINANT TRANSPORT

bed sediment processes and the overlying water column.

Since capping as a control technology by its very nature has to be considered for environments that are relatively physically quiescent, the need to understand how bioturbation controls the rate of contaminant transport out of the sediment is further emphasized. Various studies have shown that bioturbation increases the rate at which sediment constituents move into the overlying water column. Tessenow [ 3 6 ] ,for instance, observed a four- to five-fold increase in the rate of silica flux from the sediment in the presence of Chironomus plumosus larval at densities of 100 m-2. Aller [32],in his review of the literature, found that the solute transport diffusion coefficients were typically 10 to 100 times highei than bulk sediment molecular diffusion coefficients when in the presence of bioturbation. Riedel et al. [23]found that the polychaete, Nereis succinea, affected the distribution and flux of arsenic by the production of irrigated burrows. The increase in effective surface area and the activities of N . succinea increased the diffusion of arsenic by approximately a factor of five. Aller and Yingst [23]reported that in the presence of the deposit feeding polychaete, Heteromastis jilt onnis, and bivalves, Tellina texana and Macoma balt ica, C1- was effectively transported two to five times faster than it would have been by molecular diffusion alone. McCaffrey etaZ. [38] found that measured fluxes of dissolved nutrients and manganese in Narragansett Bay sediment were 10 to 1000 times greater near the surface than deep molecular diffusive fluxes. In a review of mathematical models of bioturbation, Matisoff [39] reported biodiffusion coefficients ranging from 1to 100 cmz per year in lakes and intertidal and subtidal marine and estuarine environments once corrected for biomass. More recently, Thibodeaux [40] examined the transport rates for PCBs in bed sediment of New Bedford Harbor, Massachusetts. He found the transport

A variety of processes can be responsible for the fate and transport of contaminants in bed sediment and through the sediment water interface into the water. These include: a) absorption/desorption between solids and pore water, b) molecular diffusion within the pore water, c) advective transport due to infiltration and recharge, d) advective transport due to sand ripple/wave effect, e) sediment depositionhesuspension, Q bioturbation, g) chemical reaction, h) biodegradation, i) Brownian diffusion of colloidal particles, and j) advection of colloidal particles. Some entries in the above list (a, g and h) are not transport processes; the remaining are, and the relative magnitudes of these are very site specific. In this regard, it is difficult to make general statements of the relative magnitudes. Hdwever, the examination of a few cases will convey some degree of the relative importance of these contaminant transport processes. In streams with moderate or greater water flow velocities containing little or no organic matter in the bed, there is insufficient organic matter to support the number of organisms necessary to drive the bioturbation processes. Advective processes within the bed (items c, d and j) dominate the solute molecular and Brownian diffusion processes [471.Particle deposition and suspension is also very active. Where the clay sediment bed is stable, compact and flat biological and hydraulic driven processes are minimal. In this instance, molecular diffusion is likely the only chemical transport mechanism of any significance [48].Biological and hydraulic driven processes are minimal. The last case to consider is that of organic matter-rich sediment in a large lake or estuary. In this case the presence of abundant and active organisms results in bioturbation within the bed being the dominant mechanisms even though the molecular and Brownian mechanisms are also present [40].These three examples illustrate that each sediment site is unique and that detailed information is required before contaminant transport rates can be ranked in relative importance and quantified accurately. In recent years the dredging of contaminated sediments and subsequent containment of them in subaqueous sites as well as consideration of capping of contaminated bed sediments in place to limit mobility has resulted in increasing focus on the interaction between
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FXlSTlNG C O N D I T I O U

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Figwe 7. Movement of contaminants in bed sediment with and without biotubtion.

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rates dependent on bioturbation driven processes for Aroclors 1242 and 1254 to be 300,000 to 900,000 times more rapid, respectively, than molecular driven processes when placed on a chemical pore water concentration gradient basis. Since bioturbation affects a particle transport process this is the case for all contaminants that are highly, but reversibly, sorbed onto the sediment particles. The steady state rates are directly proportional to the partition coefficients. Substantial research remains to be performed on bed sediment transport processes in order to better understand the mechanisms and resolve the apparent large differences in rates as reported above.
CONTAINMENT OF CONTAMINANTS IN BED SEDIMENT AND DREDGE SOILS BY CAPPING

Since the effects of bioturbation so strongly influence transport of contaminants from bed sediment, it follows that the removal of biological activity from contaminated sediments or dredge spoils, in the absence of any other significant physical disturbance, will result in a substantial decrease in transport dynamics. This concept has been the basis of the management of dredge spoils in many locations over the last 20 years [41]and more recently has found increasing consideration in remediating shallow subaqueous sites that have contaminated bed sediment. Figure 7 depicts how this concept works. By elevating the zone of bioturbation above the contaminated sediment, only those transport processes independent of biological activity will drive the flux of contaminants from the contaminated zone. In quiet environments molecular diffusion will become, therefore, the basis for controlling contaminant transport. In areas with highly contaminated sediment additional benefits result due to the chemical equilibrium between particle and pore water. In the case of molecular diffusion the concentration gradient is limited by solubility; whereas, no such thermodynamic constraint applies to particle driven processes like bioturbation. In order to determine the viability of capping as a solution for containing contaminants in dredge spoils and in contaminated bed sediment one must first consider the characteristics of the benthic community and the physical environment as well as the contaminant transport dynamics that may potentially occur in the specific site. We suggest you first approach the problem by considering the significant dynamics of transport in the bed sediment. An initial framework for this evaluation is provided (Table 1). In the first place one must understand the physical environment to determine whether or not under present conditions mass transport in a highly energetic environment could be the major influence on transport of contaminants. If it is determined that the physical environment is relatively low energy then the chances for cap stability are increased and an understanding of bioturbation there-

TABLE 1. FRAMEWORK FOR ENGINEERING DESIGN CRITERIA

* Develop First Order Understanding of:

-Physical Environment: Literature Research, Field Studies -Endemic Benthic Community: Literature Research --Contaminant Transport Dynamics (Vignette Models, Thibodeaux, et ul., [42]) * Ground Truth Assumptions -Field Studies of Benthic Community: Importance of Exceptions

fore more critical. Next an examination of the endemic benthic community through a literature search or through observations by an experienced benthic scientist should allow a first order of approximation of the types and numbers of organisms and potential depth of bioturbation. Once information is collected on the biotic and abiotic factors that will potentially affect the success of capping, a scenario or vignette model [42] or similar construct to synthesize this information is then applied to describe and provide first order estimates of transport phenomena. Once screening has been completed, design of the cap including its composition and depth will require detailed field studies of the sediment column and bioturbating community. While consideration of generalities about depth of bioturbation, i.e., the majority of activities restricted to the top 20 cm, are adequate to ascertain whether capping may be viable, those species which may potentially occur below 20 cm should be identified. Information must be gathered on any species which have the potential to burrow deeper than 20 cm and their density and frequency of occurrence documented. This evaluation should lead to the design of a cap that will preclude the vast majority of benthic organisms from contact with the contaminated sediment or dredge spoil layer. It is suggested that detailed ecological studies in the subject site as well as nearby similar environments be made to account for all species that might ultimately recolonize the cap. In addition, it is important to conduct coring studies and examine the vertical distribution of the contaminant under present conditions. Through examination of thin layer cores one can observe the relative effects of ongoing bioturbation in terms of how well mixed the upper strata are and can, through examination of the contaminant concentration gradient diffusion tail at depth, gain insight on the rate of diffusion in the absence of biaturbation. Once these data are collected a numercial model characterizing the situation that will result after capping should be developed. This model should take into consideration important biological as well as physical and chemical factors to allow an evaluation of resultant rates of flux of Contaminants from the bed sediment or dredge spoils. In addition bench scale studies can be conducted to verify conclusions resulting from field studies and models. For several years Brannon and others [43-451 have conducted microcosm or chamber studies of proposed caps used for dredge spoils. They have examined transport rates of tracers and contaminants both with and in the absence of bioturbation. Formica et d., [46] through use of thin layer bench scale studies, has examined microscale contaminant transport in the laboratory. In these studies a microcosm of the environmental situation is established in the laboratory and at periodical intervals a thin section of the test sediment bed is taken by microtome for analysis and evaluation of contaminant migration. Using these techniques it should be possible to determine the appropriateness of isolating the bioturbated layer from the contaminated zone as a strategy for reducing Contaminant transport. These same studies should also lead to conclusions regarding the resultant flux of contaminants to the environment due to chemical diffusion or other mechanisms after capping. This information will enable the development of predicted exposure route models to ascertain risk to human health or the environment, if any, remaining after capping is completed.
LITERATURE CITED

-Thin Layer Corings: 1-2 cm strata -Develop Numerical Model of Contaminant Transport * Bench Scale Studies -Microcosm or Chamber Studies u lu Brannon, et ul. [43,44] -Thin Layer Experiments a lo Formica et ul. [46]

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