Macrofaunal Burrows and Irrigation in Marine Sediment ... · classes in marine sediments are...

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Macrofaunal Burrows and Irrigation in MarineSediment: Microbiological and BiogeochemicalInteractions

E. Kristensen and J. E. Kostka

Abstract

Construction and maintenance of burrows by macrofauna have large implications forthe microbiology and biogeochemistry of marine sediments. Although a wealth of newinformation has become available during the last few decades, there are still significantgaps in our knowledge. In this chapter, we review the current understanding of howthe structure and function of irrigated burrows affect the composition of microbial com-munities and associated biogeochemical processes. Although a general relationship isobserved between burrow depth and diameter (inhabitant width), it is difficult to classifyburrow architecture in relation to the function and trophic mode of macrofaunal inhabi-tants. Trophic mode (suspension-feeding versus deposit-feeding) appears to controlburrow wall structure and irrigation rate and thus the exchange of solutes betweensediment porewaters and the overlying water. The associated translocation of electronacceptors into and inhibitory metabolites out of the sediment in turn affects diageneticreactions. It is well established that irrigated burrows enhance total microbial metabolismby stimulating oxic (e.g. respiration) and suboxic (e.g. nitrification–denitrification and ironreduction) reactions in the surrounding sediment. In contrast, the impacts of burrow-generated changes to diffusion scales on anoxic processes like sulfate reduction are lessclear. Sediments surrounding burrow structures likely support unique microbial communi-ties that differ from those in surficial sediments due to large differences in environmentalconditions. Biogeochemical evidence clearly indicates that the activity and abundance ofmicroorganisms are elevated around burrows. However, the mechanisms controllingmicrobially mediated geochemical reactions in the burrow zone remain understudied,and very little information is available to assess the impacts of burrow environments onthe community structure or diversity of microorganisms. Therefore, we cannot yet gener-alize about direct relationships between burrows, irrigation and the distribution of micro-organisms. However, much progress is already being made through the use of new andexciting experimental tools, such as microsensors and cultivation-independent moleculartechniques.

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The Ecogeomorphology of Tidal MarshesCoastal and Estuarine Studies 59Copyright 2004 by the American Geophysical Union10.1029/59CE04

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Introduction

Near-surface marine sediments are perforated by burrow structures in various stages ofexcavation, construction, maintenance, and disrepair. They are constructed and inhabitedfor discrete but discernable time periods and subsequently modified, abandoned for morefavorable locations, or otherwise emptied by forcible removal of the inhabitant [Diazand Cutter, 2001]. The morphology and function of infaunal burrows vary considerablyamong benthic invertebrates, from simple unbranched vertical supporting shafts or tubeswith one opening at the surface to complex and highly branched networks of funnelsand chambers inhabited by several generations of inhabitants. Burrows function as a refugeprotecting the usually soft-bodied invertebrates from predation and environmentalextremes. The burrow structures also provide physical support for the digging and feedingactivities of the burrow inhabitants, while the harsh chemical environment deep in burrowsmust be counteracted by active or passive irrigation of burrow water. Many burrow-dwellers have partly solved the latter problem by coating the burrow walls with a secretedlining of various types, ranging from thin mucus layers to thick tube walls impermeable toboth advection and diffusion. The burrow linings, on the other hand, provide an attractiveenvironment for abundant meiofaunal and microbial communities adapted to life in steepchemical gradients.

Most macroinfauna actively rework the sediment and irrigate their burrow structures.Although reworking may affect substantial amounts of sediment and visually affect theseabed topography, the less apparent irrigation of burrows with overlying water is usuallyvolumetrically orders of magnitude greater [Aller, 1982]. The renewal of burrow waterassociated with irrigation serves several essential purposes for the animals, such as gaseousexchange, food transport, gamete transport, transport of environmental stimuli, andremoval of metabolites. However, irrigation is also an important factor controlling micro-bial processes within sediments. By enhancing the exchange of solutes between the sedi-ment and overlying water, infaunal irrigation supplies dissolved electron acceptors, altersthe spatial and temporal distribution of microbial reactions, and lowers the buildup ofpotentially inhibitory metabolic products in sediments.

The majority of organic matter decomposition is mediated by microorganisms in marinesediments, and microbial activities are intimately coupled to physical and biogenicchanges in the diagenetic transport regime [Aller, 2001]. In general, benthic macrofaunaenhance microbial metabolism and the capacity for organic matter decomposition in sedi-ments through their effects on solute and particle transport. Redox oscillations mediatedby macrobenthos are also believed to result in faster and more complete decompositionrelative to deposits without these organisms [Sun et al., 1999]. Through the above men-tioned effects on diagenetic reactions, the coupling of macrofaunal burrowing to microbialactivities could have large impacts on the preservation of organic matter and the removalof nitrogen via coupled nitrification–denitrification in marine ecosystems.

In this chapter, we will briefly review the current state of knowledge on macrofaunal bur-row structures, irrigation and its biogeochemical consequences, and the microbiology of theburrow wall interface. Whereas much progress has been made on the ecological and bio-geochemical consequences of burrow structures, few studies have in recent years examinedthe diversity in burrow characteristics and faunal irrigation patterns. Furthermore, there isan obvious need to conduct more biogeochemical surveys using in situ approaches to avoidartifacts caused by the traditional laboratory experiments. It is also of concern that the abun-dance and community composition of microorganisms catalyzing important reactions inthe burrow zone remain largely unexplored. In future studies, macrofaunal activities suchas irrigation should be quantified by using high-resolution techniques in conjunction with

2 MACROFAUNAL BURROWS AND IRRIGATION IN MARINE SEDIMENTQ2

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characterization of the microbial community with cultivation-independent molecularapproaches. Other chapters of this book emphasize a modeling approach; we will insteadfocus on experimental evidence for macro–microorganism interactions.

Burrow Structures

A complete understanding of burrow microbiology and biogeochemistry can only beattained through a detailed characterization of these biogenic structures. Thus far, studieshave been limited to larger burrowers, while smaller species approaching meiofaunal sizehave largely been ignored. Although the morphology of large burrows is easily examinedby traditional approaches such as resin casts, many new photo- and microsensor techniquesmay be employed in future studies of small burrow structures. Even for larger macrofauna,relatively few species have been studied in sufficient detail. Environmental conditions,seasonal variations, and sediment conditions may force individuals of the same species andwithin the same geographical region to form widely different burrow structures.Conversely, geographically separated populations of the same species may through timeevolve different burrowing behaviour, which adds to the complexity of biogeochemistryin bioturbated sediments. Despite these obvious knowledge gaps, we will draw generali-zations based on the available information about burrow morphologies of common macro-benthic species and attempt to classify major burrow types. We will also provide insightinto the characteristics of burrow walls and describe how these boundaries might affectchemical interactions between the burrow environment and the surrounding sediment.

Morphology and Functional Types of Burrows

Burrow morphology is dictated by the feeding mode, activity level, body form, and sizeof the macrofaunal inhabitant as well as the environmental conditions and sediment com-position. Many invertebrate phyla living in marine environments have independentlyevolved classes, orders, genera, or species with a burrow-dwelling habit, including coe-lenterata (e.g. sea anemones and corals), nemertinea, nematoda, annelida (e.g. polychaetesand oligochaetes), mollusca (e.g. cockles and clams), arthropoda (e.g. insect larvae andcrustaceans), pogonophora, sipuncula, echiura, priapulida, phoronida, echinodermata(e.g. brittle stars and sea urchins), and hemichordata. The three most successful burrowingclasses in marine sediments are polychaeta, bivalvia, and crustacea.

The physical dimensions of macrofaunal burrows vary considerably, depending on thespecies and the environment (Table 1). The depth distribution of burrows in sedimentsvaries from a few centimeters for small species and juveniles to several decimeters formany adult polychaetes and more than 3 m for large crustaceans (e.g. mud lobsters)[Pemberton et al., 1976; Rhoads and Boyer, 1982]. On the basis of the database on pub-lished mixed layer depths, Boudreau [1998] estimated that the activities and consequentlythe bioturbation depth of burrow-dwelling organisms have a worldwide environmentallyinvariant mean of 9.8 cm. This value covers a large range and reflects the high abundanceof shallow burrowers (e.g. small species and juveniles) and the more scattered occurrenceof deep burrowers. Despite the large variation in burrow depths, the relationships betweenburrow depth (cm) and diameter (cm) for the selected species given in Table 1 show ahighly significant linear pattern (Figure 1A). The intercept at 8.6 cm suggests that the lin-earity of the relationship obtained here for adult individuals of relatively large species isprobably not valid for small and juvenile organisms; a different relationship is possible for

KRISTENSEN AND KOSTKA 3

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4 MACROFAUNAL BURROWS AND IRRIGATION IN MARINE SEDIMENT

TAB

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1,2

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CH

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9

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KRISTENSEN AND KOSTKA 5C

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19)

Rom

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zel [

1987

].

9738.qxd 3/26/05 1:38 PM

smaller burrows. This outcome is likely due to biases (intentional or otherwise) of macro-fauna ecologists for visible burrows or organisms that are easy to manipulate.Nevertheless, it is surprising that burrows of different larger species from widely differentenvironments exhibit such a highly correlated relationship between depth and diameter.Obviously, the relationship also reflects the size dependence of the organisms involved,since burrow diameters usually are closely related to the inhabitant’s width [Nickell andAtkinson, 1995]. However, no relationship is apparent between burrow depth and thelength of the inhabitant(s) in light of great variations in allometric dimensions amongtaxonomic groups, i.e. slender vermiform polychaetes versus more plump and compactcrabs (Figure 1B). But within the same species, there is usually a close relationshipbetween body length and burrowing depth, as shown for Nereis diversicolor by Esselinkand Zwarts [1989] and Upogebia omissa by Coelho et al. [2000]. However, some variationmay also occur within the same species, as Esselink and Zwarts [1989] found that N. diver-sicolor tends to dig deeper into sandy sediments than muddy ones. The significant inter-species depth–diameter relationship may instead point to the fact that only largerorganisms with a good body condition (i.e. sufficient muscular ability) can construct andefficiently irrigate deep burrows as well as move sufficiently quickly within the burrow toobtain food. Larger organisms may also be physiologically better adapted to withstandextended periods of oxygen deficiency and harsh chemical conditions, which are morelikely to occur in the water contained by deep burrows.

Some organisms construct simple unbranched vertical shafts with only one opening to thesurface (Figure 2, panel 1; Table 1). These are inhabited primarily by above-sediment filter-feeders, surface deposit-feeders, and subsurface deposit-feeders (head-down conveyor-beltfeeders). Vertical burrow structures appear impractical, as they usually are difficult to irri-gate and thus to provide a sufficient supply of oxygen. Many of the filter-feeders and surfacedeposit-feeders line their burrows with diffusively impermeable leathery or parchment-liketubes [Defretin, 1971; Aller, 1983]. Some of these species solve the oxygen problem bypumping water in and out of the tube like a water lung, while others transport oxygen to thedeeper parts of their bodies via their internal vascular system, supplied with oxygen fromthe filter or detritus-collecting organs placed in oxic water above the sediment surface


Figure 1. Relationships between burrow depth and (A) burrow diameter and (B) length ofthe burrow inhabitant. The line in A represents the least-squares linear regression of the filledsymbols according to the equation shown. The open symbols are considered outliers and arenot included in the regression.

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[Toulmond, 1991]. Many subsurface deposit-feeders, such as the sedentary polychaeteArenicola marina, have solved the oxygen problem by avoiding fine-grained and water-impermeable sediments (Figure. 2, panel 4). This polychaete prefers sandy sediments,where the irrigated water can percolate from the burrow and into the surrounding porespaces between sand grains [Riisgård and Banta, 1998]. However, some species haveevolved a form of mutualistic interaction, where individuals in dense populations supporteach other as a group and can both prevent buildup of noxious substances and supply suf-ficient oxygen for all individuals. For example, dense beds of the conveyor-belt–feedingmaldanid polychaete Clymenella torquata often produce a second oxidized layer at their


Figure 2. Schematic drawings of the most common burrow types made by marine benthicmacrofauna. (1) Vertical tube lined with a thick wall secreted by the inhabitant. Typical burrowfor many surface deposit–feeders and suspension-feeders (e.g. the sea anemone Ceriantheopsisamericanus). (2) U- or Y-shaped burrow, which may be lined with mucus. Mostly inhabited byactively irrigating surface deposit–feeders and suspension-feeders (e.g. the polychaete Nereisdiversicolor). (3) Y-shaped burrow with branching, which may exhibit mounds around the open-ings at the surface and chambers in the deep part. It may be lined with mucus. Typically inhab-ited by actively irrigating deposit-feeders and suspension-feeders (e.g. thalassinidean shrimps).(4) J-shaped burrow with feeding depression below the head of the animal buried deep in thesediment and a mound of fecal material around the tail opening at the surface. It is usually linedwith mucus. Inhabited by head-down subsurface deposit-feeders (e.g. the polychaete Arenicolamarina). (5) Highly branched and extended burrow system irrigated by tidal movements. Wallsare not lined with mucus but occasionally are plastered with plant detritus. Inhabited by inter-tidal crabs and used only as a refuge (e.g. grapsid crabs).

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feeding depth within sandy sediment columns, owing to both the depletion of organic mat-ter by selective feeding and the irrigation of the resulting coarse, highly permeable sedimentlayer [Rhoads, 1974; Aller, 1982, 2001]. Intertidal organisms, such as fiddler crabs (Ucasp.), use their vertical or J-shaped unbranched burrows only as refuge when disturbed orduring high tide. Otherwise, they move around on the sediment surface, foraging onmicroorganisms. These air-breathing crabs solve the oxygen problem during high tide byplugging their burrows and so maintaining within the burrow a pocket of air that containssufficient oxygen until the tide recedes again [de la Iglesia et al., 1994].

The most common type of burrows is U- or Y-shaped with two or more openings to thesurface (Figure 2; Table 1). These are often inhabited by deposit-feeders or within-burrowfilter-feeders and are actively irrigated. The multiple openings to the surface allow easy pas-sage of water through the burrows and thus are a simple solution to the oxygen problem.Burrows of this type are typical for many errant polychaetes, such as Nereis spp. (Figure 2,panel 2), that actively move around searching for food at the surface and occasionally formnew branches to the burrow [Davey, 1994]. Expanded forms of Y-shaped burrows are foundin many thalassinidean shrimp species [Griffis and Chavez, 1988; Dworschak, 2001]. Theyfirst construct a U-shaped burrow with inhalant and exhalant openings. Subsequently theydig vertically down from the bend of the U, creating a Y-shaped burrow with galleries andblind side-branches (Figure 2, panel 3). These burrows are some of the deepest burrowsfound for any organism. It is obvious that they easily can irrigate the upper part of the bur-row and thus solve the oxygen problem here, but the deeper branches must remain mostlyanoxic. The animal has to “hold its breath” during excursion to these parts of the burrow oralternatively switch to anaerobic metabolism. Many burrowing organisms are capable ofsurviving for some time on energetically demanding anaerobic metabolism, but they mustreturn to the oxic environments in the upper burrow or the sediment surface at frequentintervals to pay off the oxygen debt generated in the form of accumulated metabolites(organic acids) [McMahon, 1988; Toulmond, 1991]. Burrow-dwellers may also enduretoxic levels of sulfide during excursions to deep galleries of their burrows. Several speciesof polychaetes and thalassinid crustaceans, for example, have evolved physiological adapta-tions or symbiotic relationships with microbial sulfide oxidizers to protect enzymes such ascytochrome c oxidase from sulfide poisoning [Vismann, 1991; Johns et al., 1997]. A spe-cial version of the U- or Y-shaped burrow with blind branches is constructed by grapsidcrabs [Thongtham and Kristensen, 2003]. These air-breathing intertidal animals spend mostof their time during low tide foraging for litter and other forms of detritus. They only returnto their impressive burrows to seek protection from predation and environmental extremes.Their burrows are large and consist of a very complex disorganized network of branches(Figure 2, panel 5). One single burrow can extend to more than 1 m into the sedimentand cover an area of more than 1 m2. Only one adult crab usually inhabits one burrow, butnumerous juveniles and small thalassinidean shrimps construct narrow extensions ofthe main shafts. Burrows of grapsid crabs are irrigated passively by the tidal currents andgravity at low tide and are rarely anoxic.

Several attempts have been made to classify or model the architecture of particularlythalassinidean burrows in relation to the function of the burrow and the trophic mode ofthe inhabitant [deVaugelas and Buscail, 1990; Griffis and Suchanek, 1991; Nickell andAtkinson, 1995]. However, most of the models have difficulties placing all species within afixed framework due to e.g. plasticity of feeding behavior [e.g. Miller, 2001]. Furthermore,intraspecific differences in burrow morphology may be as great or greater than interspecificdifferences under varying environmental conditions. To avoid these problems, Nickell andAtkinson [1995] classified thalassinidean burrow morphologies on the basis of 12 burrowfeatures believed to be indicative of certain trophic requirements or modes (Table 2).


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Although Nickell and Atkinson mostly used a particular trophic mode in relation to eachfeature, burrows may morphologically be related to more than one feature. The individualfeatures of a burrow must be considered together with local environmental factors and ani-mal anatomy, as well as activities other than feeding (e.g. irrigation). Although the specificfeatures given in Table 2 are based on observations from thalassinidean shrimps, they arealso largely valid for and can be applied to burrow-dwelling animals of other taxonomicorigin (e.g. polychaetes).

All infaunal burrows alter sediment environments and affect microbial and geochemicalprocesses by increasing the area of contact zones between sediment and the overlyingwater. Based on measurements of burrow dimensions with consideration of the density ofindividuals and the age structure of the population, a number of studies have estimated thatthe presence of various infaunal burrows increases the sediment–water contact zone by50% to 400% (Table 3). Burrows of actively irrigating species are usually oxic, the oxygenpenetrating only a few millimeters into the surrounding sediment. However, the oxygenpenetration depth into burrows dominated by radial diffusion geometry is always less thanat the oxic sediment surface. From morphometric considerations, Fenchel [1996] esti-mated that the surface area representing burrow walls of a population of N. diversicolor(burrow diameter 4 mm) exceeds that of the overlying sediment surface by a factor of


TABLE 2. Burrow features indicative of certain trophic requirements of the inhabitant.Adapted from Nickel and Atkinson [1995].

Feature no. Description of feature

1 Surface mounds are indicative of sediment deposition at the surface via a deposit-feeding mode.

2 A tightly layered lattice suggests reworking by a subsurface deposit-feeder.3 Burrow depth can be indicative of the relative importance of surface

detritus in the food. Surface deposit-feeding dominates in shallowburrows and subsurface deposit-feeding dominates in deep burrows.

4 Subcircular tunnels develop as a result of animal movements in established,but not maintained, burrows. Suspension-feeding and subsurface deposit-feeding is not likely.

5 Chambered burrows indicate deposit-feeding, and chambers are used asstorage of surface or subsurface material.

6 The presence of large pieces of detritus may result from scavenging on the surface.

7 Oblique tunnels allow access to the sediment surface for movement of detritus or sediment and suggest a deposit-feeding trophic mode.

8 Numerous burrow openings to the surface suggests intimate contact with the surface and suggest a surface deposit-feeding mode.

9 Funnel-shaped openings enhance particle capture and suggest surface deposit-feeding mode.

10 A narrow exhalant shaft indicates a necessity for current generation toremove particles or capture particles and suggests a deposit-feeding orsuspension-feeding mode.

11 U- or Y-shaped burrows allow rapid water movement and indicate a suspension-feeding mode.

12 Circular tunnel cross-sections facilitate efficient flow and allow close fit for filter mechanisms and indicate suspension-feeding mode.

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up to 5. If the oxygen penetration depth at the sediment surface is 2 mm and that of theburrow wall is 1.5 mm, the ratio of oxic sediment volume associated with burrows is thenup to 5.2 times the volume of oxic surface sediment.

Structure of Burrow Walls

The wall lining of most infaunal tubes and burrows consists of mucoid, membranous, orparchment-like secretions, which may be encrusted with sand or shell debris. In some cases(e.g. burrowing crabs), the wall remains unlined and has a composition similar to the sur-rounding sediment or is enriched in fine particles [Dobbs and Guckert, 1988; Phillips andLovell, 1999; Bird et al., 2000]. The lining is in most cases highly enriched in organic mat-ter originating from the animal secretions as well as from plastered particles and detrituspulled into the burrows by the inhabitants feeding activities (Table 4). In a classic contribu-tion, Aller and Yingst [1978] described in detail the burrow wall of the polychaeteAmphitrite ornata. They found that the burrow wall consists of several thin-walled concen-tric cylinders, each 1.5–2 mm thick. The wall is lined on its inner side with a mucus layer~5 µm thick composed of protein-rich mucopolysaccharide. Wall layers beyond the liningare often formed from a higher percentage of small particles than is found in the surroun-ding sediment, suggesting that particle selection occurs when animals construct and main-tain tubes and burrows [Krasnow and Taghon, 1997]. The biodegradability of organic-richwall linings is highly dependent on the chemical composition and structure of the secretedand plastered material. For example, the mucopolysaccharide secretions produced by manyburrow-dwelling polychaetes (e.g. Nereis spp.) are readily degradable by microbialcommunities [Aller and Aller, 1986; Reichardt, 1988]. Structures like the fibrous, leatherycerianthin tubes of the infaunal sea anemone Ceriantheopsis americanus, on the other hand,are degraded at rates of less than 1% of fresh planktonic debris [Kristensen et al., 1991].


TABLE 3. Estimates of burrow wall surface area per unit sediment surface area for the listedpopulation densities of several species of burrowing invertebrates.

Species Population Burrow wall surface Referencea

density (m–2) area (m2 m–2)

Nereis virens 2000 1.25 1Nereis virens 700 1.50 2Nereis diversicolor 3500 3.00 3Nereis diversicolor 15000 ( juveniles) 1.50–4.00 4Callianassa bouveri 450 2.60 5Neotrypaea californiensis 50–100 0.70–1.40 6Callianassa gigas 50–100 1.60–3.10 6Callianassa subterranea 50 1.00–2.00 7Upogebia pusilla 30–80 1.00–3.00 8Upogebia omissa ~200 2.90 9Uca sp. 50–100 0.60 10Neoepisesarma versicolor 0.2 0.34 11

a (1) Hylleberg and Henriksen [1980]; (2) Kristensen [1984]; (3) Davey [1994]; (4) Fenchel [1996];(5) Dworschak and Pervesler [1988]; (6) Griffis and Chavez [1988]; (7) Witbaard and Duineveld [1989];(8) Dworschak [1983]; (9) Coelho et al. [2000]; (10) Katz [1980]; (11) Thongtham and Kristensen [2003].

9738.qxd 3/26/05 1:38 PM

The permeability of tube and burrow linings to solute diffusion can be an importantdeterminant of the chemical and biological composition of the tube or burrow habitat aswell as the surrounding sediment. Linings are variously semipermeable to solute diffusionand often are impermeable to advection under natural pressure conditions. Thus, Aller[1983] found that the diffusive permeability of linings from eight infaunal species ofmarine invertebrates is 10-40% of that in free solution. The diffusion of anions is hinderedsomewhat compared with cations, indicating that linings are negatively charged at sedi-mentary pH levels. The permeability of linings can, therefore, affect sedimentary solutedistribution differently depending on the sediment type, solute of interest, and types ofcontrolling reactions.

The radial diffusion geometry within and around irrigated burrows and tube structureslined with semipermeable mucus creates a unique chemical microenvironment deep insediments. The exact temporal and spatial patterns are highly dependent on the burrowtype and activity pattern of the infaunal species in question [Marinelli and Boudreau, 1996;Furukawa, 2001]. Frequent irrigation of burrows causes an exchange of water and associ-ated solutes between the burrow environment and surface water and thus drives a transportof reduced metabolites out of the sediment and oxidized electron acceptors into it. Thischanges both the relative dominance of oxidation–reduction reactions and distribution ofoxidized and reduced solutes as well as solids. The chemical gradients in the immediatesurroundings of actively irrigated burrows and tubes are usually steeper (Figure 3) andmore oscillating than near the sediment surface. The radial diffusion geometry does notallow oxidized solutes to penetrate deep into the wall, whereas reduced metabolites fromthe surrounding anoxic sediment are maintained at high concentrations close to the burrow[Meyers et al., 1987; Gribsholt et al., 2003]. Fenchel [1996], for example, found that thediffusive thickness of the oxic zone around burrows of N. diversicolor corresponds tobetween 40% and 70% of the diffusive thickness of the oxic layer at the sediment surface.The presence of oxygen and associated acid produced by aerobic processes may promotelocalized carbonate dissolution near burrow walls [Aller et al., 1983; Furukawa, 2001].In contrast, anoxic regions a short distance away from burrow walls may be supersaturated


TABLE 4. Organic carbon content (% dry weight) in wall linings of selected infaunal burrowsand tubes as well as in ambient sediment away from burrows. Values labeled with * are con-verted from loss on ignition by dividing by 2.

Speciesa Lining Ambient Referenceb

Amphitrite ornata (P) 1.4* 0.6* 1Nereis diversicolor (P) 0.5 0.2 2Nereis virens (P) 1.6* 0.7* 3Arenicola marina (P) 0.3 0.1 4Notomastus lobatus (P) 3.9 2.2 5Branchyoasychus americana (P) 3.3 2.0 5Balanoglossus aurantiacus (H) 1.1 1.0 5Ceriantheopsis americanus (A) 4.9 1.8 6Callichirus laviae (C) 1.1 0.1 7Upogebia major (C) 0.6 0.2 8

a (P), polychaeta; (H), hemichordata; (C), crustacea; (A) anthozoa.b (1) Aller and Yingst [1978]; (2) Kristensen [2000]; (3) Kristensen et al. [1985]; (4) Kristensen, unpubl.;(5) Steward et al. [1996]; (6) Kristensen et al. [1991]; (7) de Vaugelas and Buscail [1990]; (8) Kinoshitaet al. [2003].

9738.qxd 3/26/05 1:38 PM

with respect to carbonate minerals, causing precipitation in a zone immediately adjacentto the zone of dissolution [Bromley, 1996].

Burrow Irrigation

Most burrow-dwelling animals irrigate their burrows, but the mechanisms and speedwith which they create water currents are only known for a select number of conspicuousspecies. The magnitude and pattern of irrigation under various environmental conditionshas been quantified directly for even fewer species. Biogeochemical studies have tradi-tionally quantified irrigation and its consequences indirectly from porewater profiles byapplying various modeling approaches. The results obtained provide an excellent descri-ption of the averaged impact of irrigation on the sediment environment. However, short-term changes in irrigation and associated local impacts on burrow inhabitants, representedby the macrofauna itself and microorganisms along the burrow wall, can be evaluated onlyby close examination at the individual burrow level. Here we provide an overview ofirrigation mechanisms from representative examples. The volume of water driven bymacrofaunal pumps is closely linked to the purpose of irrigation, such as respiration andfilter-feeding. The rate of irrigation, in turn, exerts strict control on microbial processes aswell as the exchange of solutes across burrow walls and the sediment–water interface.

Irrigation Mechanisms

The mechanism by which benthic animals propel the water current through their bur-rows varies considerably within and among taxonomic groups. Because most describedmechanisms are represented within the two important burrowing classes, polychaeta andcrustacea, the following examples will focus on these classes (Figure 4).


Figure 3. Radial chemical gradients around infaunal burrows compared with the verticalgradients at the sediment–water interface. Left: Oxygen profiles associated with irrigatedartificial burrows in sandy sediment [Meyers et al., 1987]. The radial burrow profile is measuredat 10-mm sediment depth. Middle: Solid Fe(III) distribution associated with burrows of fiddlercrabs (Uca pugnax) in silty salt marsh sediment [Gribsholt et al., 2003]. The radial burrowprofile is measured at 5-cm sediment depth. Right: Concentration profiles of ammonium in porewater associated with burrows of the polychaete, Nereis virens, in sandy sediment [Kristensen,unpublished]. The radial burrow profile is measured at 10-cm sediment depth.

9738.qxd 3/26/05 1:38 PM


Figure 4. Irrigation patterns of various burrowing marine macrofauna: Nereis diversicolor[Kristensen, 2001]; Arenicola marina [Kristensen 2001]; Sabella pavonina [Wells, 1951];Amphitrite ornate [Aller and Yingst, 1978]; Callianassa subterranean [Forster and Graf, 1995].

Many errant polychaetes irrigate their burrows from head to tail by undulations of thebody in a dorso-ventral plane. The irrigation of species belonging to the genus Nereis isintermittent with active and quiescent periods in a more or less rhythmic fashion[Kristensen, 2001]. The exact irrigation cycles, however, differ between species. Nereis

9738.qxd 3/26/05 1:38 PM

virens is active for about 20% of the time with 5–10-min irrigation periods followed by20–30 min of inactivity [Scott et al., 1976; Kristensen, 1989], whereas N. diversicolor isconsiderably more active, particularly when it suspension-feeds. It also has active irrigationperiods of 5–10 min duration, but these are interrupted by only very short periods of inac-tivity in a very regular pattern, and it remains active for at least 50% of the time[Christensen et al., 2000].

Burrow irrigation by the sedentary and head-down conveyor-belt–feeding polychaeteArenicola marina is driven from tail to head by contraction and relaxation of the circularmuscles of the body wall in a peristaltic fashion. Water is drawn into the burrow throughthe tail opening at the surface and forced into the sediment in front of the head, where itpercolates up through the feeding funnel [Toulmond and Dejours, 1994]. The irrigationactivity of A. marina proceeds in 40–60-min cycles. These very regular cycles are proba-bly under the control of a pacemaker situated in the nervous system [Wells, 1949] and arelinked to the feeding and defecation cycles.

Filter-feeding sabellid polychaetes live permanently in a vertical tube in the sedimentwith only one opening at the surface. They are equipped with a tentacular crown stretchinginto the overlying water with both feeding and respiratory functions. Most sabellids canactively irrigate their tubes by waves of muscular contraction of the body wall in eitherdirection [Giangrande, 1991]. Burrow irrigation is almost continuous and water exits thetube by percolating into the surrounding deep sediment and forced by advection back tothe overlying water. The extent of tube irrigation depends on how important the crown isfor the total respiration of the worm. Species in which the crown is unimportant for respi-ratory purposes, tube irrigation is regular and continuous, and there are large spaces forwater movement through the tube. For those species where the crown supplies mostof the total respiration, the worm body fills the tube completely and rarely performs anyirrigation movements [Giangrande, 1991].

Sedentary, surface deposit-feeding polychaetes of the family Terebellidae irrigate theirburrows in a forward direction driven by piston-like or peristaltic body waves whileextending the numerous feeding tentacles at the sediment surface [Dales, 1961]. Thespecies Amphitrite ornata exhibits several irrigation patterns [Aller and Yingst, 1978]. Ingeneral, the patterns at the head end differ greatly from those at the tail end, and patternsobserved during feeding differ from those when the animal is retracted into the tube. Whenthe animals are retracted into the burrow, irrigation is detected only at the head end, as reg-ular pulses moving in and out of the burrow. Irrigation bursts are repeated ~3 timesa minute with wave generation occurring for about 15–20 s. The entire burrow is usuallyirrigated during feeding, typically showing large, single-velocity maxima with lower-velocity regions and periods of quiescence in between.

Thalassinidean shrimps irrigate their burrows for respiratory purposes, as in mostCallianassidae, or mainly for filter-feeding purposes, as in most Upogebiae [Atkinson andTaylor, 1988]. The irrigation flow is generated by rhythmic metachronal beating of threeor four pairs of abdominal appendages, the pleopods [Stamhuis and Videler, 1998]. Theintermittent pumping by the deposit-feeding Callianassa subterranea is more or lessregular, with about 2.5-min irrigation periods followed by about 40 min of rest [Forsterand Graf, 1995]. Irrigation bouts tend to be longer in Upogebiae than in Callianassidae dueto the difference in feeding strategy [Dworschak, 1981; Stamhuis and Videler, 1998].

Unlike most other burrowing macrofauna, intertidal deposit-feeding crabs (e.g. fiddlercrabs, Uca spp.) do not permanently inhabit or actively irrigate their burrows. Many ofthese species actually plug their burrow entrances to prevent flooding during tidal inund-ation [Koretsky et al., 2002]. However, abandoned and unplugged burrows may instead bepassively irrigated by tidal currents. Passive irrigation is particularly important in burrows


9738.qxd 3/26/05 1:38 PM

with more than one opening to the surface where at least one of the openings is raisedabove the surface, usually as a mound [Stieglitz et al., 2000; Munksby et al., 2002]. Awater current passing over the mound creates a pressure difference between burrow openingsand thus induces water flow through the burrow. Passive irrigation can be substantial inareas with strong currents and in large topographic features such as mounds and tidalcreeks; in some cases the results are comparable to or higher than active irrigation byanimals [Ray and Aller, 1985; Ridd, 1996].

Magnitude of Irrigation

The rate by which burrowing infauna irrigate burrows depends on several factors,including oxygen demand by the animal and the surrounding sediment, removal of toxicmetabolites and demand for food transported by the water current. The latter is particularlyimportant for suspension feeders with their need to process large amounts of water forextracting sufficient food particles (e.g. phytoplankton) from dilute suspensions [Riisgårdand Larsen, 2000]. These animals rarely have problems with access to oxygen, andmetabolites do not accumulate in their well-flushed burrows. Most deposit-feeders, on theother hand, irrigate their burrows discontinuously and at a relatively low rate. They haveno respiratory need to irrigate continuously and vigorously; they instead devote much oftheir time to ingesting sediment particles of low nutritious value. Species that are not cap-able of performing simultaneous irrigation and feeding must therefore adapt a strategy tomaximize feeding time and minimize irrigation time while still satisfying the respiratoryneed for oxygen. Many deposit-feeders may occasionally act as oxyregulators when oxy-gen levels in the overlying water are low and then spend considerably more time irrigatingfor respiratory purposes [Toulmond and Tchernigovtzeff, 1984; Wohlgemuth et al., 2000].Although no more than 5% of their total metabolic energy expenditure is devoted to themovement of water during irrigation [Riisgård and Larsen, 1995], some suspension-feeders may save energy by reducing irrigation when no or only limited food is availablein the overlying water. A few species, e.g. N. diversicolor, may under such conditions evenswitch to a deposit-feeding mode of life and then irrigate only for respiratory purposes[Riisgård, 1994].

The impact of feeding mode on irrigation at both the individual and the population levelis clearly evident from the examples given in Table 5. No deposit-feeding population, irre-spective of taxonomic group, appears capable of irrigating more than 200 L m–2 d–1, andmost species maintain an irrigation level one order of magnitude less than that.Suspension-feeders are more active and population irrigation for most species exceeds1000 L m−2 d−1, occasionally reaching levels an order of magnitude higher. This meansthat populations of suspension-feeders have the capacity to cycle a water column 1 to 10 mdeep through their burrows each day. Such intense cycling of large water masses throughnarrow channels (i.e. burrows) has significant implications for the exchange of matterbetween the overlying water and the sediment environment. Thus, reduced solutes areflushed from the sediment porewaters to the overlying water, while oxidized solutes aretransported the opposite way. Deposition of particulate organic matter, such as phyto-plankton, within the sediment can be substantial in the presence of suspension-feeders,either by sloppy feeding of the captured particles or secondarily by organic-rich mucussecretions and faecal material deposited within the sediment.

The importance of suspension-feeding is clearly emphasized from the study ofChristensen et al. [2000] on the polychaetes N. diversicolor and N. virens. Suspension-feeding individuals of N. diversicolor irrigate their burrows >3 times faster than their


9738.qxd 3/26/05 1:38 PM


TAB

LE

5.Ir

riga

tion

rate

s of

sel

ecte

d bu

rrow

-dw

ellin

g m

acro

faun

a. R

ates

are

tim

e-in

tegr

ated

and

pre

sent

ed fo

r bot

h an

ave

rage

-siz

ed in

divi

dual

and

for

the

entir

e po

pula

tion

abun

danc

es g

iven

at t

he s

peci

fied

loca

tions

. The

fee

ding

mod

e of

the

mac

rofa

una

is in

dica

ted

as w

ell a

s th

em

etho

dus

ed to

qua

ntif

y ir

riga

tion.

Spec

ies

Loc

atio

nA

bund

ance

Fe

edin

g m

ode

Irri

gatio

n ra

teR

efer

ence

a

(m–2

)In

divi

dual

Po

pula

tion

(mL

min

–1)

(L m

–2d–1

)

Ner

eis

vire

nsK

ertin

ge N

or,D

enm

ark

600

depo

sit

0.3

179

1N

erei

s di

vers

icol

orK

ertin

ge N

or,D

enm

ark

600

depo

sit

1.3

750

1N

erei

s di

vers

icol

orK

ertin

ge N

or,D

enm

ark

600

susp

ensi

on3.

127

001

Are

nico

la m

arin

aW

adde

n Se

a,N

orth

Sea

50de

posi

t1.

7–2.

212

0–16

02

Am

phit

rite

orn

ata

Cap

e C

od,U

SA10

depo

sit

1.2–

1.5

18–2

23

Dio

patr

a cu

prea

Eas

t Coa

st,U

SA10

–100

depo

sit

1.1

16–1

604

Cly

men

ella

tor

quat

aB

eauf

ort H

arbo

r,U

SA10

0–10

00de

posi

t0.

046–

605

Cha

etop

teru

s va

riop

edat

usG

ullm

arsf

jord

,Sw

eden

30–1

00su

spen

sion

1565

0–21

606

Cal

lian

assa

sub

terr

anea

Nor

th S

ea21

depo

sit

0.2

67

Cal

lian

assa

jap

onic

aY

amad

a B

ay,J

apan

20de

posi

t0.

5–1.

114

–30

8A

lphe

us m

acka

yiH

awai

i3

depo

sit

5.8

259

Upo

gebi

a pu

sill

aG

rado

Lag

oon,

Ital

y87

susp

ensi

on25

880

10U

rech

is c

aupo

Pilla

r Po

int,

USA

61su

spen

sion

260

2300

011

a(1

) C

hris

tens

en e

t al.

[200

0]; (

2) K

rüge

r [1

966]

; (3)

Alle

r an

d Y

ings

t [19

78];

(4)

Man

gum

et a

l. [1

968]

; (5)

Man

gum

[19

64];

(6)

Riis

gård

[19

89];

(7)

For

ster

and

Gra

f [1

995]

; (8)

Koi

ke a

nd M

ukai

[19

83];

(9)

Gus

t and

Har

riso

n [1

981]

; (10

) D

wor

scha

k [1

981]

; (11

) O

sovi

tz a

nd J

ulia

n [2

002]

.

9738.qxd 3/26/05 1:38 PM

non–suspension-feeding conspecifics and >10 times faster than deposit-feeding individualsof N. virens (Table 5). Consequently, high phytoplankton concentrations in the overlyingwater result in a 30-fold higher deposition of particulate organic carbon to N. diversicolorthan to N. virens sediment. Concurrently, the release of metabolites (CO2 and NH4

+) out ofthe sediment is increased severalfold in sediment with N. diversicolor compared with thatcontaining N. virens due to higher macrofaunal and microbial metabolism.

Burrow Irrigation and Solute Transport

Transport of solutes within sediments and across the sediment–water interface is basi-cally mediated by molecular diffusion, a relatively slow process driven solely by concen-tration gradients. The presence of burrowing macrofauna with active irrigation disrupts thediffusional gradients and strongly affects the transport conditions within sediments.Macrofauna facilitate the exchange of solutes between sediment porewaters and the over-lying water and influence the distribution of dissolved reactants (e.g. O2, NO3

–, and SO42–)

and products of early diagenetic reactions (e.g. CO2, NH4+, and H2S) [Aller, 2001; Meile

and Van Cappellen, 2003]. The biological enhancement of solute transport can exceed thetransport via molecular diffusion by as much as an order of magnitude (Figure 5). Theactual extent of the enhancement depends on such factors as reactivity of solutes, sedimentcomposition, and infaunal community structure [Kristensen, 2000, 2001; Aller, 2001].


Figure 5. Diffusive benthic oxygen uptake derived from microprofiles versus total oxygenuptake across the sediment–water interface measured with benthic chambers. The data are froma variety of continental shelf, continental slope, and deep-sea locations. The line labeled 1:1represents the situation where diffusive and total flux are similar, whereas the 5:1 line repre-sents the situation where the total flux is 5 times higher than the diffusive flux [modified fromMeile and Van Cappellen, 2003].

9738.qxd 3/26/05 1:38 PM

The presence of irrigated burrows transforms the otherwise vertical one-dimensional dif-fusive transport in sediments into a spatially three-dimensional vertical and radial transport.Solute transport within the sediment matrix occurs via molecular diffusion, and solutes enteror leave the sediment both at the sediment–water interface and along burrow walls. The roleof irrigation is therefore to increase the effective surface area available for exchange. Thisconcept has usually been applied to relatively water-impermeable sediments, where eddydiffusion (or porewater advection) is negligible. In recent years, however, studies havedemonstrated that advective porewater movements can occur in water-permeable, sandysediments when exposed to pressure gradients from water currents [Glud et al., 1996; Ziebiset al., 1996]. Advective porewater flows may affect biogeochemical reaction zones deepin these sediments, leading to complex redox patterns. When water currents are deflected byprotruding sediment structures at the surface, oxygenated water is forced into the sediment,generating distinct oxidized zones [Huettel et al., 1998]. This inflow must be balancedby porewater ascending from deeper sediment layers, thereby creating anoxic channelswhereby reduced solutes reach the surface. Since many burrow-dwelling invertebrates livingin sandy sediments irrigate vigorously [Vedel and Riisgård, 1993], porewater advection inexcess of molecular diffusion may also occur along burrow walls and thus enhance solutetransport. Accordingly, Kristensen and Hansen [1999] showed that porewater advectiondominates in the bioturbated zone and molecular diffusion dominates below this depth inpermeable sandy sediment inhabited by N. diversicolor; in impermeable muddy sedimentinhabited by the same species, molecular diffusion is the dominating transport throughout.

Biogeochemical Consequences of Burrow Irrigation

Our knowledge of biogeochemical processes in marine sediments has improved consid-erably within the last couple of decades. At the same time we have gained some insightinto the role of benthic fauna in carbon, sulfur, iron, and nutrient cycles. Most of the infor-mation provided in our review below has been obtained from small-scale laboratoryassays; only a few studies have used in situ approaches. Accordingly, small enclosures oncentimeter scales, either in situ (benthic chambers) or in the laboratory (core incubations),are well suited to examine the small-scale dynamics of microbial activity and fluxes acrosssediment–water interfaces. However, larger, mesoscale systems (flumes or sea-carousels)provide an effective linkage between small-scale manipulative systems and the naturalenvironment. Mesoscale approaches allow researchers to evaluate the biological andchemical interactions within entire benthic communities as well as the influence of wavesand currents for bentho-pelagic coupling and sediment biogeochemistry [Amos et al.,1992]. Both small and mesoscale enclosures can be applied successfully for studies of sedi-ment biogeochemistry, the actual choice depending on the purpose of the investigation[Asmus et al., 1998].

Microbial Reactions in Time and Space

Diagenetic reactions drive biogeochemical cycles, and conversely, the microbiology ofmarine sediments is largely defined by reactions associated with diagenesis [Jørgensen,2000]. Organic matter is degraded and remineralized via a complex web of microbially cat-alyzed reactions that can be considered in three major classes: depolymerization or hydrol-ysis, fermentation, and respiration [Capone and Kiene, 1988]. Depolymerization ofmacromolecules is believed to occur extracellularly and is carried out by a wide range of


9738.qxd 3/26/05 1:38 PM

heterotrophic bacteria. Fermentation of monomers is carried out intracellularly underanoxic conditions. Little information is available concerning the rates and pathways of thesefirst two steps in situ, and therefore the impact of burrow structures on these processes isnot well known. The terminal metabolism of organic matter through respiration is generallyconsidered to be the rate-controlling step, and therefore respiration reactions have been theones best studied. Organic matter is terminally metabolized through a sequence of respir-ation reactions or terminal-electron–accepting processes according to the amount of freeenergy the bacteria glean from each electron acceptor. Only bacteria that respire oxygen areable to mediate the complete oxidation of hydrolysis products to carbon dioxide; anaerobicbacteria depend on consortia with coexisting fermentative organisms that transform hydrol-ysis products to intermediates such as acetate and hydrogen [Canfield et al., 2005].

Rates of organic matter degradation depend on a variety of factors, including sedimen-tation rate, organic matter quality (i.e. protein, cellulose, lignin content), temperature, andother physicochemical parameters at the sediment–water interface. A vertical sequence ofterminal respiration processes is often observed in marine sediments whereby oxidants aredepleted in the order O2 > NO3

– > FeIII, MnIV > SO42– > HCO3

– (Figure 6) [Froelichet al., 1979; Canfield et al., 2005]. However, respiration pathways are not determined bythermodynamics alone. Kinetics and the availability of various electron acceptors are alsoof critical importance, leading to the spatial overlap of respiration processes. In fact, thecurrent paradigm is that respiration pathways often coexist in marine sedimentary envi-ronments because of non–steady-state conditions [Postma and Jakobsen, 1996] that maybe forced by macrofaunal activities [Kristensen, 2001; Kostka et al., 2002a, b].

Concurrent to carbon oxidation, a large portion of electron acceptor utilization is cou-pled to the reoxidation of reduced inorganic metabolites produced during remineralization[Canfield et al., 1993]; typically, 90% or more of reduced species such as sulfide, iron, andmanganese are recycled [Thamdrup and Canfield, 1996]. Thus, the recycling or reoxida-tion of respiration products often limits the supply of electron acceptors. Reoxidation mayoccur via abiotic chemical reactions, but it is often mediated by chemoautotrophicmicroorganisms [Jørgensen, 1989]. Of particular importance is the dissolved metabolitesulfide, produced from sulfate reduction. Sulfide is toxic to benthic organisms and can inextreme cases lead to defaunation of the sediment.

Of the many factors influenced by macrofauna, alteration of the diagenetic transportregime during burrow construction and irrigation is believed to have the largest impact onmicrobially mediated geochemical cycles (Figure 6) [Aller, 2001]. Ultimately, throughrespiration and reoxidation processes, diagenetic reactions are limited by the transport ofsolutes, and this is where burrows and irrigation can have a major impact on microbialcommunities and the biogeochemical processes they catalyze. Infauna affect diagenetictransport passively by increasing the sediment–water contact zone and by actively pumpingwater through irrigation or feeding activities (see above discussion and Kristensen [2001]).Analogous to conditions at the sediment surface, enhanced solute transport across burrowwalls stimulates microbial reactions around burrows. Fluid transport near the burrow wallthereby influences the rates, pathways, and extent of organic matter remineralization andnutrient cycles [Aller, 2001]. Burrow irrigation increases the supply of soluble reactants,such as electron acceptors and carbon substrates deep in sediments, while stimulating theremoval of toxic metabolites such as dissolved sulfide. Increased reoxidation and redoxoscillation through intermittent irrigation apparently leads to more efficient degradation oforganic matter and the emergence of suboxic pathways [Aller, 1994; Kristensen, 2001].

Translocation of O2 to subsurface sediment and removal of metabolites are therefore con-sidered the two most important mechanisms for the stimulation of carbon oxidation byburrowing fauna. When O2 is introduced to otherwise anoxic sediment of low microbial


9738.qxd 3/26/05 1:38 PM

activity, the decay of anaerobically refractory organic matter will be stimulated by up to afactor of 10 [Kristensen and Holmer, 2001] and thus will enhance the total sedimentarycarbon oxidation. In addition, it has been suggested that the reduced diffusion scale createdby a high abundance of irrigated burrows in sediment may enhance anaerobic degradationby (e.g.) removal of inhibitory metabolites [Aller and Aller, 1998]. However, experimentalevidence for the latter mechanism is still limited [Valdemarsen and Kristensen, 2005].

Respiration Pathways and Nutrient Cycling

Benthic-pelagic coupling is of critical importance to primary production in coastalwaters, and the majority of biogeochemical studies examining interactions between


Figure 6. Burrow of Nereis diversicolor with indications of fluxes and redox-sensitive reactions.The burrow structure has a large impact on terminal electron accepting pathways and the nitro-gen cycle, primarily due to alteration of the diagenetic transport regime. The light areas repre-sent the oxidized zone containing electron acceptors (O2, NO3

–, Mn(IV), Fe(III), SO42–). The

dark areas represent the reduced zone containing metabolites (H2O, NH4+, N2, Mn(II), Fe(II),

HS–). Arrows show various transport and reaction processes.

9738.qxd 3/26/05 1:38 PM

benthic macrofauna and microorganisms have been conducted in shallow, marine eco-systems. Therefore, here we will primarily focus on marine sediments from shallow conti-nental shelves to intertidal zones.

In coastal marine sediments rich in organic matter, oxygen is rapidly utilized and anaer-obic respiration is considered as important or frequently more important to carbon oxida-tion. Aerobic respiration has been estimated to account for roughly 50% of carbonoxidation in most coastal sediments [Thamdrup and Canfield, 2000]. Sulfate reduction onaverage contributes the remaining 50% of carbon oxidation on continental shelves[Jørgensen, 1983], but tends to be more important in many fine-grained intertidal environ-ments [Kristensen et al., 2000b; Kostka et al., 2002a,b]. However, in areas inhabited bylarge infaunal communities, microbial Fe(III) reduction can comprise up to 100% ofcarbon oxidation [Kristensen et al., 2000a; Kostka et al., 2002a; Gribsholt et al., 2003].Other respiration pathways such as nitrate reduction generally play a minor role in carbonoxidation, but denitrification may represent an important sink in the marine nitrogen cycle.

Present estimates indicate that only a small fraction of benthic oxygen consumption inshallow marine sediments is due to respiration by infauna; the fauna, in contrast, primarilyimpact oxygen consumption through irrigation. Oxygen uptake in sediments has beenshown to increase severalfold in the presence of abundant macrofauna (Figure 5)[e.g. Christensen et al., 2000, Meile and Van Cappellen, 2003]. Faunal-mediated O2 uptakemeasured in situ correlates well with faunal abundance in many open ocean areas, wherebottom water chemistry is relatively constant [Glud et al., 1994]. However, in shallowercoastal sediments, where temperature and bottom water oxygen vary seasonally and diur-nally, in situ measurements usually show no clear relationship between faunal biomass andO2 flux [Glud et al., 2003]. However, under constant conditions in the laboratory, there isa clear relationship between infaunal abundance and O2 uptake, even for intertidal sedi-ments [Tahey et al., 1994; Papaspyrou et al., submitted].

Because O2 may be consumed by a variety of processes, including respiration by aero-bic bacteria and chemical reoxidation of reduced metabolites, it has been difficult to relateany specific O2-consuming process to macrofaunal activity. Rates of biotic vs. abiotic O2consumption have been estimated from extensive measurements in conjunction with geo-chemical profiling [Canfield et al., 1993; Thamdrup and Canfield, 1996], but detailed char-acterization of infaunal community composition or activity has rarely been included.To relate aerobic respiration directly to burrow structures or irrigation, it will be necessaryto conduct careful experimentation with benthic fauna coupled with comprehensivebiogeochemical assays.

Since sulfate reduction is exclusively catalyzed by anaerobic bacteria and sulfate reduc-tion rates are easily measured with a radiotracer method, the relationship between macro-fauna and anaerobic carbon oxidation in sediments has been more evident. A large numberof studies have related the presence or abundance of macrofauna to sulfate reduction rates[Hansen et al., 1996; Banta et al., 1999; Kostka et al., 2002a,b; Gribsholt et al., 2003].However, the results thus far have been equivocal. Sulfate reduction rates in the sedimentzones immediately surrounding burrows are in some cases enhanced [Hines and Jones,1985] and have been attributed to the introduction of organic substrates by transport/excre-tion. Hansen et al. [1996] found that sulfate reduction rates were 2 times higher in theburrow wall of bivalves than in the surrounding subsurface sediments, and the ratescorrelated with viable counts of sulfate-reducing bacteria. When artificial burrows wereintroduced into the same sediments, on the other hand, a suppression of sulfate reductionactivity was observed. Kostka et al. [2002a] similarly observed a nearly complete suppres-sion of sulfate reduction rates and a predominance of microbial iron reduction in salt-marshsediments where fiddler crab burrows were abundant, while sulfate reduction dominated


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carbon oxidation in adjacent sediments where crab burrows were absent. From high-resolution radial profiles in fiddler crab burrow walls in the same salt marsh, Gribsholt et al.[2003] showed low sulfate reduction rates in parallel with high iron reduction rates withina few centimeters of the burrow wall. The conclusion of these salt marsh studies was that arapid iron cycle facilitated by reoxidation in the burrow wall allowed iron-reducing bacte-ria to outcompete sulfate-reducers for carbon substrates. At present, it appears that sulfatereduction may be stimulated or inhibited by macrofaunal burrows depending on a host ofenvironmental parameters, including sediment geochemistry, porosity, and the ecology ofburrow-dwelling organisms. The exact mechanisms by which burrows impact sulfate reduc-tion and other anaerobic carbon oxidation pathways remain to be elucidated.

The steep chemical gradients and potential overlap between electron acceptors(e.g. oxygen) and reduced metabolites (e.g. sulfide, ammonium and reduced iron) aroundmacrofaunal burrows and tubes provide an ideal environment for the growth ofchemolithoautotrophs. This is confirmed by a higher potential dark CO2 fixation alongpolychaete burrow walls than in surface sediment (Table 5; Reichardt [1986, 1988]).Evidence from the literature for enhanced chemolithoautotrophic activities in infaunalburrows and tubes is mainly related to nitrification, although it has been argued that certainsulfur-oxidizing thiobacilli and Beggiatoa often are responsible for most of the chemoau-totrophic activity [Reichardt, 1988]. Mayer et al. [1995] concluded from their own studiesand a review of the existing literature that most macrofaunal burrows exhibit nitrificationpotentials exceeding those from adjacent and surface sediment. Of 11 species examined,burrows or tubes of 9 species had nitrification potentials exceeding surface sediment byfactors of 1.5 to 61. Nitrification potentials in burrow walls appear to be regulated by thediffusive access of ammonium from the ambient sediment and supplies of oxygen viairrigation by the burrow inhabitant. Thus, Mayer et al. [1995] found that nitrificationpotentials correlated positively with both the bulk sediment ammonium concentration andthe macrofaunal irrigation behaviour. Furthermore, it has been argued that high nitrifica-tion potentials in macrofaunal burrows are related to an association of nitrifying bacteriawith the fine-particulate and organic-rich wall linings [Henriksen et al., 1983; Kristensenet al., 1985]. The strong association to fine particles is linked to the pH-buffering capacityof clay and silt particles, which is likely to help retain an optimal pH for nitrifiers, and tothe high availability of ammonium derived from microbial nitrogen mineralization of theorganic particles [Canfield et al., 2005]. This information is discussed below.

The role of macrofauna in nitrification is a key linkage between the mineralization oforganic nitrogen and the removal of nitrogen via denitrification. Indeed, denitrification isenhanced in the presence of burrowing macrofauna [Nielsen et al., 2004]. Macrofaunaburrows may also be linked to the nitrogen cycle indirectly via their impact on anaerobicrespiration pathways. Dissolved sulfide was shown to inhibit both nitrification and deni-trification in laboratory cultures and in marine sediments [Joye and Hollibaugh, 1995;Joye, 2002]. As outlined above, a change in the partitioning of respiration pathways fromsulfate to iron reduction has been observed in the burrow wall of fiddler crabs, and the shiftin carbon oxidation pathways was accompanied by a large decrease in the accumulation ofsulfide [Kostka et al., 2002b; Gribsholt et al., 2003]. In a subsequent study of the same salt-marsh sediments by Dollhopf et al. [2005b], nitrification and denitrification potential rateswere strongly correlated with one another and with macrofaunal burrow abundance, indi-cating that coupled nitrification–denitrification was enhanced by macrofaunal burrowingactivity (Figure 7). The distribution of nitrifying bacteria, as determined by quantitativePCR, was further shown to have a high positive correlation to Fe(III) and a negativecorrelation to dissolved sulfide. Laboratory slurry incubations supported field data,confirming that increased amounts of Fe(III) relieved sulfide inhibition of nitrification.


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Thus, it was proposed that burrow structures are an important driving factor in the C, N,Fe, and S cycles of the salt marsh, facilitating solute transport and continually recyclingelectron acceptors critical to both the oxidation of organic matter and coupled nitrification–denitrification. Enhanced iron cycling in the burrow zone may amplify the positive effectsof solute transport on coupled nitrification–denitrification by reacting with sulfides,thereby stimulating nitrogen removal in coastal ecosystems.


Figure 7. Influence of burrow abundance on (A) nitrification potential, (B) denitrification potential,and (C) the distribution of nitrifying bacteria as determined by gene copy number of ammoniamonooxygenase A in sediments of a Georgia salt marsh. TS, Tall Spartina habitat (314–352burrows m–2); CB, Creek bank (58–184 burrows m–2); SS, Short Spartina (53–99 burrows m–2).Winter samples have a W prefix, summer samples have no prefix. Error bars represent the standarderror of the rate calculated from linear regression of duplicate assays. g wet, grams (wet weight).From Dollhopf et al. [2004, in press].

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Impact of Irrigated Burrows on Sedimentary Microorganisms

The presence of burrows lined with organic coatings of various composition combinedwith the steep chemical gradients in their immediately surrounding sediment createmicroenvironments with distinctive and species-specific microbial communities and reac-tion properties. Furthermore, the fairly stable physico-chemical environment inburrows/tubes compared to the more frequently disturbed surface sediment allows for thedevelopment of complex microbial biofilms [Steward et al., 1996; Phillips and Lovell,1999]. This can lead to the formation of microbial communities fundamentally differentfrom the nearby surface and subsurface sediments, with substantial bacterial diversity,density and activity [Marinelli et al., 2002; Kinoshita et al., 2003; Lucas et al., 2003].

Though the biogeochemical consequences of burrow structures and irrigation have beenwell documented, the detailed interactions and mechanisms by which burrows affectmicrobial community composition and activity remain relatively unknown. Knowledgegaps may be at least partly blamed on the complexity of the burrow zone. Microbialcommunities in the burrow wall will respond to sediment characteristics, physicochemicalconditions of the surrounding environment, and the species-specific ecology of the infaunaover a range of spatial and temporal scales. The response of the microbial community tochanges in solute transport, for example, is likely to occur rapidly (seconds to hours) andvery close (micrometers to millimeters) to the burrow wall. Simply due to their small sizeand large phylogenetic diversity, detecting microbial community response to even largegeochemical gradients remains challenging

Knowledge Gaps: Microbiology of Burrow Structures

Especially regarding the abundance and community composition of microorganismsinhabiting the burrow wall–sediment interface, relatively few studies have been performedand the field has currently generated more questions than answers. We review existingknowledge below. However, prior to summarizing the field, it may be helpful to discusscurrent gaps in our knowledge.

Microbiological studies of the burrow wall environment have been diverse and thus farrelatively simple, involving mostly biomass or established activity determinations. Largevariations in the definition of the burrow interface make definitive or quantitative compar-isons difficult. The water, tube, lining, and walls of macrofaunal burrows have all beensampled at varying spatial scales. The majority of studies have compared microbial com-munities in macrofaunal tubes or burrow walls with those of surface sediments or ambientsediments. Ambient sediment is usually defined as anoxic sediment at least 1 to 5 cm inradial distance from any burrow, but many past studies have considered the “surface” as0 to 2 cm deep, while the “subsurface” is usually at >5 cm deep. Although the burrows ofmajor irrigating infauna (polychaetes, crustaceans, and bivalves) have been represented inpast work, systematic comparisons between the burrows of different organisms are, asshown earlier, diffuse and not always consistent.

The majority of studies to date have been limited geographically to shallow, coastal sedi-ments, most studies focusing on intertidal environments and relatively few on the subtidal areasfrom the continental shelf to the deep sea. Considering the huge diversity of microorganismslikely to be present in marine sediments [Keller and Zengler, 2004] and in burrows in particu-lar, most studies have investigated general bacterial populations; only a few functional groups(aerobes, sulfate-reducers, iron-reducers) have been characterized in the burrow wall.

The microbiology of burrows must also be considered in the context of broader limitationsin our knowledge of the microbial ecology of marine sediments. Clearly, more information


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is available on abundance/biomass and diversity of functional groups in marine sedimentsthan has been studied in relation to infaunal burrows. However, the general knowledge ofmicrobial community composition in marine sediments remains limited and consensus hasnot been reached with regard to the variation in community structure with environmentalparameters [Keller and Zengler, 2004]. For example, studies of burrow interfaces have beencarried out under a range of different sediment characteristics (porosity, density, grain sizedistribution, organic matter content). Such characteristics are well known to drasticallyimpact biogeochemical processes in marine sediments, and yet no information has beencompiled on the influence of sediment characteristics on microbial community structure.Therefore, differences in the activity and community composition of microbial communitiesdue to macrofaunal burrows cannot be effectively separated from those differences attributedto sediment characteristics at this time.

Abundance and Biomass

The majority of microbial studies carried out in burrow environments have employedsimple measurements of abundance or biomass, and the perception has been that the stand-ing stock of microorganisms is much larger in or near (within 1 cm) the burrow wall thanin the surroundings. When considered from a microbiological standpoint, an analysis ofthe literature to date reveals relatively mild effects of burrow structures on the overallabundance of microorganisms (Table 6). The largest enhancement of abundance as directcounts in the burrow wall relative to that in surrounding sediments was by a factor of 3


TABLE 6. Selected examples of microbiology of burrow wall sediments (≤1 cm from burrowand including burrow structure itself) relative to that of surrounding “ambient” sediments ofequal depth (values are given as the ratio of burrow wall:ambient).

Species Sediment Abundance Biomass Activity Refa

Direct Viable

Polychaeta:Capitella capitata sand 0.9 1Arenicola marina sand 1.3 12.2 5.0 2Notomastus lobatus sand 5.7 3Branchyoasychus americana sand 8.6 3Amphicteis sp. mud 1.8 4

Bivalvia:Arctica islandica sand 1.4 5Mya arenaria mud 1.7 10.0 2.3 6

Crustacea:Biffarius arenosus sand 1.1 2.5 7Callianassa trilobata sand 9.7 8Upogebia major mud 1.8 1.4 9

Hemichordata:Balanoglossus aurantiacus sand 3.4 3

a(1) Alongi [1985]; (2) Reichardt [1988]; (3) Steward et al. [1996]; (4) Aller and Aller [1986]; (5) Bussmannand Reichardt [1991]; (6) Hansen et al. [1996]; (7) Bird et al. [2000]; (8) Dobbs and Guckert [1988];(9) Kinoshita et al. [2003].

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[Lucas et al., 2003], and half of the studies employing direct counting procedures observedno enhancement of abundance in the burrow wall [Reichardt, 1988; Bird et al., 2000]. Thelack of strong bacterial enrichment in the burrow wall can be explained by extensive meio-faunal grazing along the wall [Wetzel et al., 1995]. Another explanation could be thatalthough overall cell numbers are not enhanced in the burrow wall, the growth and activityof certain functional groups may be stimulated.

Measurements of microbial biomass as phospholipid fatty acids (PLFA) or ATP (adeno-sine triphosphate) have revealed an enhanced “active” bacterial biomass in the burrow wall(Table 6). Nearly all previous investigations have observed 2 to 10 times higher PLFA orATP biomass in the burrow wall relative to that in ambient sediments [Aller and Yingst,1978; Steward et al., 1996]. Because both PLFA and ATP are rapidly turned over in marinesediments, these cellular components should represent a sensitive measure of “viable”microbial biomass, whereas direct counts will include both live and dead cells.Microorganisms grow on an exponential scale and thus a factor of 2 to 10 difference innumber is generally not considered large. However, the database remains small and theresults clearly indicate a substantial enhancement of viable microbial biomass in theburrow wall zone. Viable counts of specific functional groups of organisms support thisconclusion. Hansen et al. [1996] observed an order of magnitude higher counts of sulfate-reducers while Reichardt [1988] found 106 times higher counts of cultivatable aerobes inthe burrow wall than in the surrounding sediments.

Microbial Community Structure

Few studies have related microbial community composition to the unique biogeo-chemistry of burrows, but early evidence suggests that microbial communities are uniquelyadapted to environmental conditions in the burrow wall. Several studies have compared themicrobial communities of burrow structures to those of surrounding sediments by profil-ing of PLFA extracted from bacterial membranes. Steward et al. [1996] used quantitativecomparisons supported by multivariate statistical analysis to show that the microbial com-munities of polychaete burrows in an intertidal sand flat were markedly different fromthose of surrounding surface and subsurface sediment. The authors concluded thatmicroorganisms were responding to the physicochemical properties of the burrows.Significant differences in the PLFA profiles of prokaryotes associated with the burrowbetween wall and surrounding sediment were also observed in a sandy tidal flat inhabitedby Thalassinidean crustaceans on the Gulf Coast of Florida. Functional groups of bacteriawere also shown to differ as the PLFA biomass attributed to the sulfate-reducing bacteriawas elevated in the burrow wall [Dobbs and Guckert, 1988]. In a study by Marinelli et al.[2002], artificial burrows or mimics were devised to examine the influence of irrigation,tube composition, and tube residence time on microbial communities. Burrow mimics sup-ported the development of microbial assemblages that were similar to those observed innatural burrows in terms of the relative abundance and community composition [Stewardet al., 1996]. Dominant fatty acids, including those attributed to sulfate-reducing bacteria,accumulated in response to longer mimic residence times and were negatively impacted bytreatment with a bacterial exopolymer, which suggests that burrow residence time and tubecomposition influence colonization by prokaryotes. Irrigation frequency was not shown tobe an important factor in the structuring of microbial biofilms on burrow mimics.However, the relatively short duration and colder temperatures of the experiment werecited as potential reasons why irrigation frequency did not affect microbial communitystructure. Not all studies of PLFAs have found the burrow environment to contain a unique


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microbial community. Bird et al. [2000] observed no significant difference in microbialcommunity structure between the burrow wall of Thalassinidean shrimp and surroundingsand-flat sediments. Limitations in the PLFA profiling method might explain the contra-dictory results.

While PLFA profiling is sensitive and quantitative, and the biomarker analysis can becarried out using automated instrumentation, a drawback of this technology is that PLFAsignatures provide a relatively low-resolution fingerprint of microbial functional groups.Prokaryotic PLFAs must be separated from those of eukaryotes, and the phylogenetic iden-tification of bacterial groups is limited to the family level or above. Only certain groupsof bacteria can be identified with confidence such as Gram positives, Gram negatives,aerobes, anaerobes, and sulfate-reducers.

Nucleic acid–based (DNA, RNA) methods for profiling microbial communities remaintedious and suffer from some additional drawbacks of their own. However, DNA or RNAsequences provide a much higher resolution for the identification of microbial groups tothe genus or species level. In addition, a plethora of new techniques within this field prom-ise to revolutionize microbial community characterization in sediments. Not only havemethods become more reproducible and quantitative, but it is now possible to relate thephysiology or activity of certain microbial groups to their in situ identity. These cultivation-independent molecular techniques are still in their infancy for the analysis of burrowmicrobial communities. To our knowledge, only a few research groups have examined thecommunity fingerprint or diversity of burrow wall microbial communities using nucleicacid–based technologies. Lucas et al. [2003] investigated the microbial assemblages ofmuddy sediments in a salt marsh by examining the community fingerprint of 5S rRNA.They used the relative intensity and number of 5S rRNA bands as operational taxonomicunits to estimate microbial diversity with the Shannon index. Microbial diversity wasfound to differ between sediment heavily colonized by polychaetes and uncolonized sedi-ments. However, the authors could not obtain enough sample size to specifically examinecommunities of the burrow wall. In addition, the method did not allow for the identifica-tion of specific microbial groups.

More recent studies have used the 16S rRNA gene as a biomarker for determination ofmicrobial community composition associated with burrow structures. Matsui et al. [2004]utilized clone libraries, denaturing gradient gel electrophoresis (DGGE), and DNA–DNAhybridization methods to provide a thorough analysis of community composition in thetubes constructed by the polychaete genus Diopatra. Although large variations wereobserved in community composition between the tubes and the surrounding sediment, aprincipal components analysis of DGGE banding patterns showed some distinct trends.Bacterial communities in tubes from sandy sediment differed substantially from those intubes of muddy sediment. The difference in community structure was observed for bothgeneral bacterial communities and specifically for the sulfate-reducers. In a similar study,Papaspyrou et al. [submitted] showed that molecular fingerprints of bacteria within andaround burrows of nereidid polychaetes (Nereis spp.) and a Callianassid mud shrimp(Pestarella tyrrhena) provided large differences between surface, burrow wall, and ambientsediment. Furthermore, the bacterial communities along burrow walls were more similar tothose in the ambient anoxic sediment and showed less seasonal change than those in the sur-face sediment. Accordingly, it was concluded that burrow walls contain distinct microbialcommunities and should not be considered simple extensions of the sediment surface.

Only a single study has targeted the “active” bacteria associated with burrow structures byusing quantitative RNA-based profiling. Dollhopf et al. [2005a] used reverse transcriptionreal-time PCR to quantify the 16S rRNA of anaerobes in a radial profile through the burrowwall of a fiddler crab in muddy salt-marsh sediment. RNA extracts from pooled sediment


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sections of the radial profile were examined with primer sets specific for predominant generaof sulfate- and iron-reducing bacteria. Since RNA is degraded more rapidly than DNA insediments, RNA-based profiling should detect the “active” microbial community members.The 16S rRNA of all anaerobic groups was at a maximum within 1 cm of the burrow wall,indicating the communities were most active or stimulated there (Figure 8). Vertical depthprofiles further revealed that the rRNA of known iron-reducing bacteria was more abundantin Fe(III)-rich sediments where fiddler crab burrows are abundant and microbial Fe(III)reduction has been shown to be a predominant carbon oxidation pathway.

Conclusions and Recommendations for Future Research

Ecological and sedimentological work conducted during the last few decades has pro-vided solid evidence for how infauna construct and maintain burrows. Although individualspecies generally inhabit specific burrow types, the geographical variation in sedimentcharacteristics often results in intraspecific differences in burrow morphology that are asgreat or greater than interspecific differences. Accordingly, most models that attempt toclassify all burrowing species based on burrow characteristics (such as morphology, func-tion, and trophic mode) have difficulties and are generally of little practical use.

The diffusivity of burrow and tube linings combined with irrigation creates a uniquechemical microenvironment deep in sediments. The exact temporal and spatial patterns ofchemical gradients are highly dependent on the burrow type and activity patterns of theinfaunal species present. Microbial communities in the more oxidized zones surroundinginfaunal burrows are often considered equivalent to communities present in surficial sedi-ments. However, environmental conditions in the burrow wall fundamentally differ from


Figure 8. Quantification of the “active” anaerobic microbial groups in a radial profile througha fiddler crab burrow wall in muddy salt-marsh sediment using reverse transcription real-timePCR of extracted 16S rRNA [Dollhopf et al., 2004, submitted]. The percentage 16S rRNA copynumbers of iron-reducing bacteria of the Desulfuromonadales (DMC), Desulfuromonadaceae(DSF), and Geobacteraceae (DFL) groups are represented by the left axis; the percentage copynumber of the sulfate-reducing bacteria of the Desulfococcus (DCC) group is represented by theright axis.

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those at the sediment surface. The sediment surface is physically unstable over the shortterm due to advective forces (tides, currents) and chemically stable over longer time scalesdue to exchange with overlying waters [Kristensen, 2001]. In contrast, burrows are morephysically stable over their lifetimes (days to weeks) but are chemically unstable overshorter time scales (minutes) due to intermittent irrigation. Burrow walls are thereforelikely to support the growth of unique microbial communities that differ considerably fromthose in both the oxic surface and the surrounding anoxic sediment.

Overall, the microbiology associated with irrigated burrow structures is in its infancy.Biogeochemical evidence and rate measurements have clearly shown that microbial acti-vity is elevated in the burrow zone. Viable cell counts and biomass determinations supportbiogeochemical evidence to indicate that microorganisms exhibit an elevated metabolicpotential in or near the burrow wall. However, the mechanisms and the parameters con-trolling microbially mediated geochemical reactions in the burrow zone remain under-studied, and very little information is available to assess the impacts of burrowenvironments on the community structure or diversity of microorganisms. The “active”microbial communities that catalyze important geochemical reactions in the burrow zoneremain therefore largely unknown.

Consequently, it is too early to generalize about direct relationships between burrowstructures, irrigation activity, and the distribution of sedimentary microorganisms.However, new and exciting experimental tools in biogeochemistry and microbiology areavailable with which these questions may be addressed. High-resolution geochemical tech-niques such as microsensors and other in situ approaches should be employed and tightlycoupled to sampling for microbial parameters. For both the abundance and diversity ofmicroorganisms, future research should employ more robust, cultivation-independentmolecular techniques and statistical comparisons. Manipulative studies remain valuablebut need to be carried out in a close collaboration between multidisciplinary groups (ben-thic ecologists, geochemists, and microbiologists). Macrofaunal activities such as burrow-ing or irrigation and geochemical reaction rates should be quantified and directly relatedto microbial parameters quantified in the same sediment. Such collaborative experimentshave been attempted in mesocosms with artificial burrows but not with real organisms andunder in situ conditions. Burrow–microorganism interactions have the potential to largelyimpact global biogeochemical cycles and yet this potential has not been realized.

Acknowledgments. This work was supported by grants from the Danish ScienceResearch Foundation (Grant 21020463) to E.K. and the U.S. National Science Foundation(OCE-0424967) to J.E.K.

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