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Bioirrigation Modeling in Experimental Benthic Mesocosms

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Bioirrigation Modeling in Experimental Benthic Mesocosms Journalof Marine Research, 59, 417–452, 2001 Bioirrigationmodeling in experimentalbenthic mesocosms byYokoFurukawa 1,SamuelJ. Bentley 2 andDawn L.Lavoie 1 ABSTRACT Burrowirrigation by benthic infauna affects chemical mass transfer regimes in marine and estuarinesediments. The bioirrigation facilitates rapid exchange of solutes between oxygenated overlyingwater and anoxic pore water, and thus promotes biogeochemical reactions that include degradationof sedimentary organic matter and reoxidation of reduced species. A comprehensive understandingof chemical mass transfer processes in aquatic sediments thus requires a proper treatmentof bioirrigation. We investigated bioirrigation processes during early diagenesis using laboratorybenthic mesocosms. Bioirrigation was carried out in the mesocosms by Schizocardium sp.,a funnel-feedingenteropneust hemichordate that builds and ventilates a U-shapedburrow. Interpretationof thelaboratory results was aided by atwo-dimensionalmulticomponent model for transportand reactions that explicitly accounts for the depth-dependent distribution of burrows as wellas the chemical mass transfers in theimmediate vicinity of burrow walls. Our study shows that bioirrigationsigni cantly affects the spatial distributions of pore water solutes. Moreover, bioirriga- tionpromotes burrow walls to be the site of steepgeochemical gradients and rapid chemical mass transfer.Our results also indicate that the exchange function, a,widelyused in one-dimensional bioirrigationmodeling, can accurately describe the bioirrigation regimes if itsdepth attenuation is coupledto the depth-dependent distribution of burrows. In addition, this study shows that the multicomponent2D reaction-transport model is ausefulresearch tool that can be used to critically evaluatecommon biogeochemical assumptions such as theprescribed depth dependencies of organic matterdegradation rate and C/ Nratio,as wellas thelackof macrofaunalcontribution of metabolites tothe porewater. 1.Introduction Manymacroinvertebrates inhabit benthic boundary layers in marine and estuarine environments.Some of these animals construct burrows as their habitats, which they ventilatewith O 2-richoverlying water (i.e.,bioirrigation). Consequently, O 2 and other electronacceptors are introduced to sediments that are well away from water-sediment interface(WSI), andmetabolites such as dissolved inorganic carbon and ammonium are removedto overlying water. Previous studies have recognized the signi cance of this bioirrigationprocess in sedimentary early diagenesis (e.g., Aller, 1982; Kristensen, 1988; Marinelli,1992; Martin and Banta, 1992; Emerson et al., 1984;Aller and Aller, 1998; 1.Naval Research Laboratory,Sea oor Sciences Branch,Stennis Space Center,Mississippi, 39529, U.S.A. email:yoko.furukawa@ nrlssc.navy.mil 2.Louisiana State University,Coastal StudiesInstitute, Baton Rouge, Louisiana, 70803, U.S.A. 417 418 Journalof MarineResearch [59, 3 Figure1. The schematic model geometry of Aller’s cylindermodel (Aller, 1980), with r1 5 burrow radius, and r2 5 half-distancebetween burrows. Furukawa et al., 2000).In these studies, bioirrigation is found to quantitativelyaffect the microbialremineralization reactions and solute uxes.Comprehensive understanding of thechemical mass transferin marine and estuarine environments thus requires a mechanis- ticand quantitative understanding of thebioirrigation processes. Today,the common quantitative treatment of bioirrigation involves a mathematical expressionof one-dimensionalnonlocal exchange (e.g., Emerson et al., 1984;Boudreau, 1984;Martin and Banta, 1992). The measure for thisexchange, nonlocal exchange function a,isusually described as a simplefunction (e.g., constant, linear decrease, exponentialdecay) of depth. Whereas this modeling strategy often produces agreement betweenmeasured and modeled depth pro les of solutes(e.g., Matisof and Wang, 1998; Kristensenand Hansen, 1999; Schlu ¨ter et al., 2000),the mathematical formulae and “best-t” parameter values for a donot allow deconvolution of actual mechanistic steps involvedin the bioirrigation processes (Meile et al., 2001).Moreover, this type of 1D treatmentgives little insights to the lateral spatial variability in chemical mass transfer regimesassociated with the burrows. Themost mechanistic model treatment of bioirrigationto datewas establishedby Aller (1980,1982, 1984). In his so-called cylinder model, bioirrigated sediment is idealizedas a collectionof laterallyclose-packed, identical cylinders, each with a cylindricalvoid space (i.e.,burrow) ofan identical geometry in the center (Fig. 1). The outer surface of each microenvironment(i.e., r 5 r2)representsthe midpoint between two adjacent burrows, andthus the point of zero radial ux.In this model, bioirrigation is mathematically expressedas the radial diffusive exchange of solutesperpendicular to theburrow wall. The concentrationof agivensolute at a givenposition at a giventime, Cx,r,t,canbe determined bythe equation that describes vertical diffusion perpendicular to the water-sediment 2001] Furukawaet al.: Bioirrigation modeling 419 interface(WSI), radialdiffusion perpendicular to the burrow wall, and net rate of productionor consumptionof thesolute due to biogeochemicalreactions: ]Cx,r,t ] Dsw ]Cx,r,t 1 ] Dsw ]Cx,r,t w 5 w 1 rw 1 R (1) ]t ]x X u2 ]x D r ]r X u2 ]r D (Aller,1980; Boudreau, 1997, p. 63) where w [ porosity, t [ time, Dsw [ diffusion coefcient of the solute in seawater, u [ diffusivetortuosity, and R [ overallrate of production/consumptionreactions. The diffusive tortuosity term in the equation can be replacedby aporosityexpression using the following empirical correlation: u2 5 1 2 ln ~w2! (2) (Boudreau,1997, p. 132).The model originally presented by Aller(1980) assumes that the burrowwater composition is always the same as that of overlying water (i.e., 100% irrigation).The original model geometry also assumes that all burrows have the identical radiusand depth extent, and are equally spaced. Boudreau and Marinelli (1994) extended themodel to allow periodic, discontinuous irrigation in whichthe burrow water composi- tionstarts to equilibrate with surrounding pore water while the burrows are not actively irrigated.This model re ects the observations that many infauna species go through alternatingventilation and rest cycles (e.g., Kristensen, 2000). Furukawa et al. (2001) incorporatedthe metabolite contribution by burrowingmacrofauna into the discontinuous irrigationmodel. Theadvantage to such a 2Dmodeling approach over the use of simple 1D nonlocal exchangefunctions is that 2D models allow us to quantify the spatial and temporal heterogeneityin sedimentgeochemistry. For example,Aller (1980) showed the widerange oflateralvariability in pore water compositionsas a functionof distancefrom themodel burrowwall using the original cylinder model. Marinelli and Boudreau (1996) used the discontinuousirrigation model as well as an idealized laboratory microenvironment to illustratethe steep gradients in redox and pH conditions in the immediate vicinity of burrowwalls. Furukawa et al. (2001)calculated the possible lateral variability in the thermodynamicstabilities of calciumcarbonate minerals due to bioirrigation and infauna metabolismusing the model that incorporated discontinuous irrigation and macrofaunal metaboliteproduction. Whereasthe original cylinder model and its derivatives provide insights to the processes thatoccur in associationwith burrows, their application to actualsediments is limited.This ispartlybecause of theassumption that all burrows are vertical and havethe identical depth extent.In reality, more than one species of burrowing infauna usually inhabit a given sedimentaryarea, creating burrows of variousdepth extents and geometries (e.g., D’ Andrea andLopez, 1997; Levin et al., 1999).Many species of burrowing infauna are known to createburrows with complex geometry that may not be adequately approximated by verticalcylinders (e.g., Davey, 1994; Rowden and Jones, 1995; Ziebis et al., 1996; Scaps et 420 Journalof MarineResearch [59, 3 al., 1998).A bioirrigationmodel would be moreapplicable to actualsediments if itwere ableto account for thevariable depth extents and tilt angles of burrows. Our strategytoward the quantitative and mechanistic understanding of bioirrigationthus involvesthe construction of a2Dbioirrigationmodel, with a simultaneousdata collection inlaboratory benthic mesocosms. The model formulation takes into account the parameters thatwere previouslyconsidered (e.g., burrow radius, number of burrowsper unit area of seabed;Aller, 1980; Boudreau and Marinelli, 1994; Marinelli and Boudreau, 1996). In addition,our model considers other parameters that are important in the adequate descriptionof eldand laboratory observations, such as the depth-dependent distribution ofburrows and burrow tilt angles. The laboratory experiments provide directly measured datafor constrainingthe model geometry and boundary chemical values. They also supply depthpro les of solute species that are used to evaluatethe model outputs. Consequently, thesimulation results demonstrate the quantitative signi cance of depth-dependent bioirri- gationin terms of netchemical mass transfer.Moreover, the model results illustrate the lateralvariability in chemical mass transferregimes especially in the vicinity of burrow walls.This study also demonstrates the model as an evaluation tool for common assumptionsused in biogeochemical studies of early diagenesis, such as the prescribed depthdependencies of organicmatter
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