benthic fauna and biogeochemical processes in marine sediments

Nitrogen Cycling in Coastal Marine EnvironmentsEdited by T. H. Blackburn and 1. S91rensen((d 1988 SCOPE. Published by John Wiley & Sons Ltd

CHAPTER 12

Benthic Fauna and BiogeochemicalProcesses in Marine Sediments:Microbial Activities and Fluxes

ERIK KRISTENSEN

12.1 INTRODUCTION

A great variety of benthic animals disturbs the texture and chemistry of coastalmarine sediments. Many of the effects result from the changes that these animalsproduce in transport processes. Sediment reworking by feeding, burrowingand construction activity influence particle transport (Rhoads, 1974;Yingst andRhoads, 1980)while water and solute transport is affected mostly by ventilation(Kristensen, 1984). The resulting physical and chemical changes in habitatconditions are known to enhance microbial activities and growth rates (Newell,1965; Fenchel, 1972; Hylleberg, 1975; Hargrave, 1976; Rhoads et ai., 1977;Kristensen et ai., 1985). Such microbial 'gardening' effects may result from: (1)transfer of newly sedimented reactive particles to depth in the sediment; (2)supplyof electron-donors and electron-acceptors by upward transport of reduced anddownward transfer of oxidized compounds; (3) concentration of organic-richparticles into faecal pellets, which are colonized by microorganisms followingdefaecation; and (4) breakdown of aggregates by grazing activities, therebyincreasing particle surface area for microbial colonization and maintainingmicrobial populations in a high-productivity phase of rapid growth.

The purpose of this chapter is to evaluate the effectsof benthic animals on thequantitatively most important microbial nitrogen transformations (e.g. miner-alization, nitrification and denitrification) in coastal marine sediments. Theemphasis is on measured reaction rates and fluxesof dissolved inorganic nitrogenassociated with animal activity. During the past decade there has beenconsiderable progress in the understanding of the influence of biogenic activitieson physical, chemical and biological conditions in marine sediments. Thedevelopment of more precise microbiological techniques has resulted in a betterlocalizationof microbialactivity in bioturbatedsediments. Biogenic particle

276 Nitrogen Cycling in Coastal Marine Environments

mixing willonly be treated briefly here, although such activity can be importantfor the redistribution of reactive organic matter in sediments (e.g. McCall andTevesz, 1982).The major emphasis will be on small-scale temporal and spatialvariations of microbial processes, and fluxes of inorganic nitrogen associatedwith biogenic structures like burrow-or tube-walls and faecal pellets ofinfaunal animals.

12.2 SEDIMENT REWORKING

Macrofaunal reworking, i.e.burrow construction and feeding, affectsthe stabilityand composition of coastal marine sediments. This may cause changes in therates and mechanisms of diagenic reactions. Various infaunal animals disturb thesediment structure differently depending on their specific feeding type, mobilityand life cycle. Typical 'conveyor-belt' feeders (Rhoads, 1974), such as thepolychaetes Clymenella torquata and Heteromastus filiformis, are intense per-turbers. They live head-down in relatively permanent vertical burrows, feedingon deposits at some depth. Anoxic material is transported as faecal castings to theoxic sediment surface. Surface deposit-feeding polychaetes (e.g. Nereis spp. andAmphitrite spp.),crustaceans (e.g.Corophiumspp.) and bivalves (e.g.Macoma spp.and Abra spp.), however, rework the sediment more by burrowing than byfeeding, because they primarily depend on fresh detritus at the surface as a foodsource. The surface deposit-feeding polychaetes and crustaceans commonly livein more or less permanent V-shaped burrows or tubes with at least two openingsto the surface, while bivalves usually live permanently buried with their siphonsextended to the surface.

In the absence of perturbing macrofauna, reactive organic detritus associatedwith a high primary production is normally deposited in a relatively labile state asa flocculent layer on the sediment surface. Here a rapid preferential mineraliz-ation of nitrogen occurs (Blackburn, 1980).This is mediated through the activityof benthic microorganisms and animals that constitute the aerobic detritus foodchain. Below the oxic zone the rate of mineralization by anaerobic processes (e.g.fermentation, denitrification and sulphate reduction) is slowed by a decline in thenutritional quality of the organic matter with depth and age in the sediment. Thispattern is reflected in a considerable decrease in microbial numbers withincreasing depth (Rublee, 1982;19>rgensen,1983).When macrofauna are presenttheir activities cause redistribution of organic detritus at a rate different fromsedimentation. The use of radioactive tracers has proved successful in obtainingindirect estimates of such sediment mixing events (Aller and Cochran, 1976;Smethie et al., 1981;Smith and Schafer, 1984).Because of their varied half-lives,e.g.from 24.1days for 234Thto 5730years for 14C,the different isotopes are usefulover a range of different depth and time scales. The decay rate of an isotopelargely determines both the penetration pattern of reactive organic matter in asediment and the absolute quantity of a constituent decomposing at any given

Microbial Activities and Fluxes 277

Totol 210pb octivity (dpm/g)

0 4 8 12 16 0 4 8 12 16 0 4 8 12 16

3

E2

~ 10E'5'"'"-E~c.'"0

20

2

Figure 12.1. Total 210Pbactivity distribution in three sediment cores from the NewFoundland continental slope. Core 1 is relatively undisturbed. Core 2 is mixed bybioturbation in the upper 4cm from 74 infaunal species, induding 33 polychaetespecies. Core 3 has two subsurface maxima due to deep burrowers: the crustaceanMunidopsis and the burrowing sea anemone Edwardsia (after Smith and Schafer,1984)

depth. Evidence of sediment mixing by the use oftracers is known to be consistentwith the life habits of the infaunal animals (Figure 12.1).'Conveyor-belt' feedersnormally cause homogeneous downward transport of reactive organic matterinto older sediment strata, a phenomenon that has been used to estimatesediment mixing rates by a diffusion analogue mixing model (Goldberg andKoide, 1962;Guinasso and Schink, 1975).For a variety of surface deposit feedersthe redistribution of organic particles appears, at least on short time scales,unsuited for description by a sediment diffusion coefficient. These animalstransport organic material from the surface to their relatively permanent tubes orburrows by feeding and ventilation. By analogy with particle tracers, suchdownward advective transport of reactive detritus may result in secondarymaxima of reactive organic matter at depth in the sediment (Figure 12.1).

12.3 VENTILATION

Ventilation of burrows and tubes is a major factor controlling biogeochemicalprocesses occurring in sediments (Kristensen, 1984,1985).Benthic macroinverte-brates, buried in the sediment, generally pump water through their burrows byactive ventilation. Such renewal of burrow water serves several importantpurposes for the animals, such as: (1) gaseous exchange; (2) food transport; (3)gamete transport; (4) transport of environmental stimuli; and (5) removal ofmetabolites. Infaunal ventilation activity usually produces an increased trans-port of water and solutes in and out of the sediment, while biogenic particle


reworking is responsible for a mixing of reactive organic matter. Ventilation isvolumetrically much greater than particle reworking.

Many studies have reported on ventilation rhythms in infaunal polychaetes(e.g.Wells, 1949;Mangum, 1964;Scott et al., 1976;Kristensen, 1983),crustaceans(e.g. Foster-Smith and Shillaker, 1977; Dworschak, 1981; Gust and Harrison,1981) and bivalves (e.g. Hamwi and Haskin, 1969; Vahl, 1972). Measurement andquantification of infaunal ventilation has proved a difficult task. Severalmechanic and electronic methods have been employed, such as kymographs(Wells, 1949),thermistors (Scott et al., 1975),pressure transducers (Foster-Smithand Shillaker, 1977) and electromagnetic flowmeters (Kristensen, 1981). Theelectromagnetic flowmeter, that has been used in biogeochemical studies, isapparently one of the most precise and reliable methods (Kristensen, 1984).Themajority of ventilation experiments have been performed in artificial bur-rows, e.g. plastic or glass tubes, for physiological purposes. Such approachesare not suited for most biogeochemical studies because the measured ventilationrates generally are higher than those found in natural sediment (Table 12.1).Glass tubes are useful when animal contribution to sediment oxygen and

ammonium flux are to be determined. Use of plastic tubes should be avoidedbecause plasticizers might affect the animals (Kristensen, in preparation).However, excellent techniques have been developed to quantify the ventilationactivity and its function in natural sediment (Shumway and Davenport, 1977;Kristensen, 1983). These have revealed that most infaunal animals showintermittent ventilation, interrupted by periods of rest, in a more or less rhythmicfashion. By the use of a V-core system (Figure 12.2)Kristensen (1984)found thatthe average duration of ventilation periods in the polychaete Nereis virens isabout 7 minutes followed by a rest periods of about 28 minutes; ventilationoccurring'" 20% of the time. The rate appears to be directly proportional to bodyweight for this and related species, i.e. by knowing the biomass and weight-specificventilation rate the volume of water ventilated by a population of Nereiscan be estimated. The total water volume ventilated by a population of N ereis

Table 12.1. Ventilation rate (ml H2O g-l h -I) by infaunal polychaetes

Artificialtubes

Naturalsediment References

N ereis virensN ereis succineaNereis diversicolorNereis diversicolorArenicola marinaArenicola marinaAbarenicola affinisClymenella torquata

101183360149

14-37

1937

Kristensen, 1983Kristensen, 1983Kristensen, 1981Foster-Smith, 1978van Dam, 1937Kruger, 1966Barrow and Wells, 1982Mangum, 1964

10-136060

Microbial Activities and Fluxes

2g ww Nereis virens

10 20

Time {minI

30 40

Figure 12.2. Upper: experimental V-core used to quantify theventilation current and its transport functions for polychaetes (e.g.Nereis spp.) in natural sediment. A: Site for excurrent watersampling; B: silicone rubber ports for sampling of burrow water.Arrows indicate the direction of water movement. Cables from the

flowprobe are connected to an electromagnetic flowmeter. Lower:example of ventilation pattern and rate for a 2 g wet weightindividual of Nereis virens

279

7

6

5

4

'c: 3.E

E 2

c:.g

10- 0c:Q)>

-1

-2L0


virens(700individuals or 228 g wet weight per m2) at 16°C is then -100 litresm-2 d-1, equivalentto a turnover in the burrows of about 150times per day.

12.4 PROPERTIES OF BURROWS

Although the composition and geometrical structure ofinfaunal burrow walls aredifferent from surface sediment, the presence of burrows can be viewed as anextension of the sediment-water interface. Kristensen (1984) estimated that anestuarine population of the polychaete Nereis virens (700 individuals per m2)extends the contact zone between sediment and water -150%, i.e. below each m2sediment surface there is 1.5m2 nereid burrow walls. It is clear that such burrowstructures increase the complexity of microbial activities and solutes in sedi-ments. However, the relatively permanent burrows of macroinvertebrates maynot be regarded as being biogeochemically similar to the oxic surface layer ofsediments. The topography of surface sediments is continually disturbed bymacrofaunal feeding, current, and wave-mediated particle transport. Suchdisturbances are, on short time scales, generally absent in the circular andcommonly mucus-lined burrow walls. On the other hand, the concentration andfluxes of various solutes may be considered relatively constant at the sedimentsurface, in contrast to the periodically ventilated burrows.

The abundant burrows and tubes found in coastal sediments are usually linedwith layers of organic material. The permeability ofthe linings, to either advectiveflow or solute diffusion, can be an important determinant of chemistry both insurrounding sediment and in the burrow habitat. Various infaunal macroinverte-brates produce their own specific linings, ranging from parchment-like tubes ofthe polychaete Chaetopterus variopedatus to the thin mucus lining of nereidpolychaetes that readily disintegrates upon handling. Infaunal bivalves also linetheir burrows with mucus, which prevents sediment-fouling of the ventilationcurrent and clogging of the gills.The linings secreted by infaunal polychaetes areusually composed ofmucopolysaccharides rich in sulphate and phosphate (Zola,1967;Muzii, 1968).In many cases the mucus lining are supplied and mixed with

Table 12.2. Average silt + clay « 63Jlm) content inburrow linings and away from the lining in Amphitriteornata (after Aller and Yingst, 1978) and Nereis virens(after Kristensen et al., 1985)burrows

Radial sample PercentageSpecies zone silt + clay

Amphitrite ornata 0-3mm 22.1ambient 14.7

N ereis virens 0-2mm 9.610-15 mm 1.6


small particles obtained from the sediment surface as reported for the polychaetesAmphitrite ornata (Aller and Yingst, 1978)and Nereis virens (Kristensen et al.,1985).This explains a commonly observed increase in the abundance of smallparticles in the burrow wall (Table 12.2).The nitrogen-rich detritus particles may,for surface deposit feeders, be transported from the sediment surface to theburrow by the feeding activities. Evidence suggests, however, that at least a part ofthe particles is transported in suspension via the ventilation current. Thesuspended particles probably stick to, or are adsorbed to, the mucus lining; thusHarley (1950)described that the polychaete N ereis diversicoloroccasionally usesthe secreted mucus as a filter-feeding funnel. Continued construction andmaintenance of the lining is often reflected in a slight lateral movement oforganic-rich wall structures. This has been observed as an increased content oforganic matter several millimetres away from the burrow wall (Figure 12.3).

Oxygen penetration into sediments is important for microbial nitrogentransformations, such as nitrification and denitrification (Hansen et aI., 1981;Andersen et al., 1984; S~rensen, 1984). Oxygen is commonly consumed in thesurface layer of coastal sediments diffusing to a depth of only a few millimetres(J~rgensen and Revsbech, 1985).The supply of oxygen in burrows is primarilydependent on the ventilation activity of the burrow inhabitants. The intermittentventilation pattern observed for the majority of infaunal species may promote

00

Organic content (%)2 3, 4

.5 10

.<=CiQ)

00 Burrow wall

. Surface

i /'

\ /'

Vo.

~ 5EE

cQ)

E:0Q)

(/)

15 I I I

Figure 12.3. Radial burrow wall (Nereis virens) and vert-ical surface profiles of organic matter, measured as loss onignition (500°C). (AfterKristensenet al., 1985.)


very variableoxygenconditionsin the burrows.For nereidpolychaetestheoxygen level approachesthat of the surfacewater during active ventilationperiods,but during the usually long restingperiodsoxygenconsumptionby theburrow inhabitant and wall microbesrapidly exhaustthe oxygen(Figure 12.4).Such conditions, together with the radial diffusion geometry, produce a variableand generally low oxygen penetration into the wall sediment which may steepenthe gradientsofmicrobialprocessesand solutes.Hyllebergand Henriksen(1980),however, estimated that the increase in oxic sediment volume due to bioturbationis 30-50% with the polychaete Nereis virens and 100-150% with the crustaceanCorophium volutator (2000 and 6000 individuals per m2, respectively) whenassuming an oxygen penetration of 6 and 2 mm into surface sediment and burrowwalls, respectively.

Oxygen availability in burrow environments is of vital importance for themacrofaunal inhabitants, but it may also affectgrowth and population sizesof theassociated organisms. The abundance of meio- and microorganisms alongsideinfaunal burrows is normally quantitatively and qualitatively different from boththe ambient anoxic and the oxic surface sediment. For example, the density of

v R v R100

80

c.Q

~ 60::J0II>

CQ)a>

~ 400

Q)a>0C~ 20Q;

Q.

10 20 30Time (min)

40 50 600

Figure 12.4. A representation of oxygen concentration changes inthe centre of a Nereis virens burrow. N. virens ventilates the burrow-7 minutes, where 44% oxygen is extracted from the water, followedby 25 to 30 minutes rest period, where oxygen is depleted. Vand R indicate ventilation and resting periods, respectively. (AfterKristensen, 1985.)


Table 12.3. Abundance of small zoobenthos (Nematoda, Oligochaeta, Polychaeta,Copepoda, Turbellaria) per cm3 around burrows of infaunal polychaetes, away fromburrows in ambient sediment at the same depth and from the oxic sediment surface.Diversity was determined by the Shannon-Wiener index: H = - ~Piln2Pi

meiofauna in burrow walls is usually high (Table 12.3);in some instances higherthan at the surface and in others lower, but it is generally higher than in theambient sediment (Aller and Yingst, 1978;Reise, 1981).Thus when surface andsubsurface meiofauna are taken together, biogenic structures will be expected toaccount for 10-50% of the total abundance. The species composition ofmeiofauna measured as diversity, however, is highest at the sediment surface andgenerally much lower in both burrow walls and ambient anoxic sediment(Table 12.3)where Nematodes are the dominating group. These observations onmeiofaunal abundance indicate that the burrow environment may result ingrowth of specificbiological assemblages, possibly induced by the high variabilityof solutes such as oxygen and nutrients in the burrow wall. Meiofaunal grazing ofbacteria may also influence microbial decomposition (Fenchel and Harrison,1976),which will further accentuate spatial variations.

12.5 BENTHIC FAUNA AND MINERALIZATION

The downward mixing of reactive detritus, either by homogeneous reworking oradvective transport into burrows, affectbulk mineralization profiles. The net rateof nitrogen mineralization in sediments is generally considered equivalent to therate of ammonium production minus the rate of ammonium incorporation intocells (Blackburn, 1979; Blackburn this volume). The fraction of producedammonium that is not incorporated has three possible fates: (1) entering thesediment ammonium pool, either in porewater solution or adsorbed to particles;(2) transport to the overlying water; and (3) oxidation.

Only a few studies have dealt with the stimulatory effect of infauna onmineralization processes. An elevated ammonium production has, however, beenobserved at depth, in bioturbated compared to non-bioturbated coastal sedi-ments (Blackburnand Henriksen, 1983).This may diminish the role of the

Burrows Ambient Surface

Diver- Diver- Diver-Species Density sity Density sity Density sity

Nereis diversicolor" 94 0.458 12 0.488 150 0.439N ereis virens" 352 0.075 9 0.104 76 0.612Arenicola marina" 457 0.385 70 0.169 258 0.759Amphitrite ornatab 78 0.130 6 - 554 0.669

a From Reise (1981); b From Aller and Yingst (1978).

---


Net NH: production (nmol cm-3d-' )0 50 100

2 _/'-~I ~o

i /---//°-,

r0

0 Bioturbated- Non-bioturbated

4E~~ 6Q)

E'6~ 8_!:..c0. 10Q)0

12

14

Figure 12.5. Rates of net ammonium pro-duction at two stations from Danish coastalwaters. The non-bioturbated station is rela-tively undisturbed by biogenic activities. Thebioturbated station experiences biogenicactivity by a Brissopsis-Chiajei community.(After Blackburn and Henriksen, 1983.)

oxidized surface layer in bulk mineralization (Figure 12.5).The highly organicsilty-mucus wall lining of infaunal burrows should, together with downwardtransport of detrital particles, provide a substrate for microbial growth deep inthe sediment. Kristensen and Blackburn (1987)have observed an increased loss oforganic matter due to the polychaete Nereis virens in lOcm deep microcosms.Over a 94-day period they found that carbon and nitrogen mineralization in thepresence of worms was stimulated by a factor of 2.6 and 1.6, respectively,compared to controls (Figure 12.6).The average rate of nitrogen mineralizationin the presence and absence of Nereis virens was 76 and 47nmolcm-3d-1,resp~ctively. Feeding activities by this surface deposit-feeding worm wasresponsible for 20-40% of the loss. Billen (1978)similarly found the ingestion andassimilation of detritus by infaunal communities in North Sea coastal sedimentsto be responsible for about 20% of the bulk nitrogen recycling in both oxic andanoxic sediment.

The level of infaunal stimulation is dependent upon the sediment type; thehigher the organic content, the more important the stimulation (Henriksen et ai.,1983).Ventilation of surface water into the burrows supplies electron-acceptors(e.g. oxygen, nitrate and sulphate) and removes possible inhibitory metabolites


x 10-'%

0 2 3 20 30 60 70 80

2

E 4S"EQ)

E:g 6<n.S-'=c.~ 8

10

Figure 12.6. Profiles of particulate organic nitrogen (paN), particulateorganic carbon (PaC) and loss on ignition (La I) in two sediment systemsincubated over a 94-day period. The dotted lines represent the initialcondition. The continuous lines represent the organic content in a bio-turbated system (-1400 Nereis virensjm2) and a non-bioturbated systemafter 94 days (after Kristensen and Blackburn, 1987)

(e.g. ammonium and sulphide). The HzS, which is produced by sulphatereduction, is known to inhibit microbial processes; the addition of 10mMsulphideto a sediment inhibits the sulphate reduction by 50%, while 20 mM stops itcompletely (J~rgensen, 1983).Thus, in an organic-rich sediment, where the build-up of sulphide is expected to be much higher than in a poor sediment, thestimulation of microbial processes by infaunal activities obviously must be moreefficient.

The increased mineralization and ammonium production in the presence ofinfauna should be expected to increase the porewater ammonium concentration.No such increase occurs, however, and biogenic activity is actually known todecrease bulk sediment ammonium concentration (Figure 12.7)by an increasedtransport out of the sediment due to ventilation activities (McCaffrey et aI., 1980;Klump and Martens, 1981; Blackburn and Henriksen, 1983;Kristensen, 1984,1985).The flux of solutes across the wall of infaunal burrows has been determinedin a few cases either by sampling of water directly from the burrows duringintertidal periods when ventilation could not take place (Aller and Yingst, 1978)or by measurement of the effiuxout of individual burrows by the V-core system(Kristensen, 1984, 1985) and relating this to the surface area of burrow walls.

- , . 'I .// I " " ,1.,0 .;,0

A.. Non-bioturbated /1 A:0.Ii! l \!0 Bioturbated

II!08 I

\ ii

0 .,

\\ i \ Ii0. I 0.' 0 ..

//1 I / II

\\!o . 0 .1

\1 / Ii0 . I 08' 0 .1

I I .

PON POC LOI

I '/ I I /, . ., ,

286

E3

c~ 6i5ill<1>

.!:

~ 8ill

0

Nitrogen Cycling in Coastal Marine Environments

Ammonium concentration (I-'M)

0 100 200 300 400 500 600 700

.I~IIII

/0 .~ Without

,,-,refS

\ With .\\~mi' i

r i\ \° .

2

4

10

12

Figure 12.7. Porewater profiles of ammonium in sedi-ment from Norsminde Fjord, Denmark. Closed symbolsare from cores without infauna. Open symbols representcores from sediment with 700 Nereis virensjm2. (AfterKristensen, 1984.)

Table 12.4. Ammonium flux across walls of infaunalburrows

a Aller and Yingst (1978); bAiler et al. (1983); C Kristensen(1984).

These studies have revealed that the flux of ammonium across burrow walls(Table 12.4) are of similar magnitude to that reported for nearshore surfacesediments (Table 12.5).Nitrification within the burrows may, however, consumea substantial part of the produced ammonium. The diffusiveflux from surround-ing sediment into burrows appears to be of minor importance at steady-state

Temperature Ammonium flux

Species (°C) (!lmolm - 2 h - 1)

Amphitrite ornata" 22 35Onuphisjennerib 24 23

Upogebia affinisb 24 63N ere is virensc 16 64

Table 12.5. In situ flux of ammonium and nitrate from different depth regimes. Theinorganic nitrogen flux is given as percentages of the annual phytoplankton demand

(0 )

- 30:2"

:J..

,~. -'.~....,--

~ 2°r.

/,' .:: ..:J .D ~ .E0"$

40

.f; 010

L.20 30

E 100~ l (b)0EE 800

'0 /

2::/'/'.

.9 60

~~ 40c0(,)

100 200Time (min)

Figure 12.8. Ammonium build-up: (a)in a burrow of Nereisvirens during ventilatory rest period (after Kristensen, 1984);and(b)in burrowsof a Amphitrite ornata population exposedon a tidal flat (after Aller and Yingst, 1978)

300

Temper- Ammonium Nitrate PercentageDepth ature flux (flmol flux (flmol of annual

Location (m) (cC) m-2h-1) m-2h-1) demand

Eel Pond" 2 20 85 0 93Neuse River Estuaryb 3 22 219 0 26Narragansett BayC 6-7 15 100 -

Buzzards Bay" 17 16 124 3 101New York Bightd 23 12 53 19 42Belt Seae 15-25 10 21 19 29-50Western Kattegate 14-25 10 29 14 30- 72Eastern Kattegate 43-65 10 33 8 53Atlanticf 2200 3 0.95 -0.95Atlanticf 2750 3 0.61 -0.80

a Rowe et al. (1975); b Fisher et al. (1982); C Nixon et al. (1976); d Florek and Rowe (1983);e Blackburn and Henriksen (1983); f Smith et al. (1978).

50


conditions compared to the production processes. Kristensen (1984) observedthat the total ammonium flux out of nereid burrows is independent ofconcentration ranging from 2 to 90JiMin the overlying water (bulk porewaterconcentration; 200-300 JiM).This implies that mineralization in the burrowwalls and animal excretion are the major sources for ammonium flux out ofburrows. The pattern of ammonium build-up in burrows during periods ofventilatory rest is usually linear, but may show a logarithmic build-up initially, asobservedin burrowsofNereisvirens(Figure 12.8).Thelogarithmicbuild-uphaspartly been attributed to excretion by the animals (Kristensen, 1984).The highrate at the start of a rest period could be a 'time lag'; the animals excretingammonium that had accumulated in the previous high metabolic state of activeventilation. The slower rate of accumulation later on could primarily be the resultof mineralization and diffusion from the burrow wall. Alternatively, suchconcentration patterns may reflect non-steady-state build-up of ammonium inthe presence of a high capacity for adsorption by the burrow wall lining.

The populations of burrow systems have, for a variety of infaunal species, beenfound to constitute 17-90% (average 72%) of the bulk ammonium flux fromcoastal sediments and 34-80% (average 69%) of the total inorganic nitrogen flux(ammonium + nitrate) (Table 12.6).These values are, however, highly dependentupon the organic content of the sediment, nitrification activity, animal speciesand density. The direct excretion by the macrofauna may account for a

. Kristensen (1985);b Henriksen et al. (1983); C Koike and Mukai (1983).

Table 12.6. Flux of ammonium from bulk sediment, animal + burrow systems andexcretion by the infaunal animals. Values in parentheses are the total inorganic nitrogenflux (ammonium + nitrate)

AnimalBulk flux + burrow Excretion

Density Temper- (Ilmol (Ilmol (IlmolSpecies (m- 2) ature CC) m-Zh-l) m-zh-l) m-Zh-l)

PolychaetaN ereis virens' 600 16 100(132) 79(45) 32N ereis virensb 2000 15 239(206) 205(166) 128Arenicola

marinab 140 15 224(192) 190(158) 70

CrustaceaCallianassa

japonicac 20 20 120 20 -

Corophiumvolutatorb 6000 15 43 (79) 33(62) 41

BivalviaMacoma

balticab 500 15 100(130) 90(90) 90


substantial part of the inorganic nitrogen flux from burrows; thus 24-69%(average 46%) (Table 12.6).The observed variation between excretion rates forvarious infaunal animals may be caused by differences in morphology and lifehabit combined with different rates of nitrogen removal by denitrification in theburrow walls.

12.6 NITRIFICATION AND DENITRIFICATION IN BURROWS

Vertical profiles of nitrate in undisturbed sediments usually depend upon theoxygen distribution. The nitrate zone is typically 1-5 cm deep, with maximumconcentration in the uppermost centimetre due to nitrification in the oxiczone (Vanderborght and Billen, 1975;Henriksen, 1980).Ventilation of burrowstructures with downward transport of oxygen in the sediment may be reflected inthe vertical profiles of nitrate by the appearance of secondary maxima insediment layers too deep to be reached by diffusion (Figure 12.9)(Grundmanisand Murray, 1977; S~rensen, 1978). This indicates that nitrification andsubsequently denitrification is occurring in the burrows of infaunal animals.

Ammonium in burrow walls will either be oxidized by autotrophic nitrifyingbacteria or pass to the burrow water and subsequently to the overlying water bythe ventilation current. It is unknown precisely to what extent ammonium isoxidized in the narrow oxic zone in the walls. This may vary according to theintermittent ventilation pattern. There is, however, strong evidence for a highpotential nitrification in burrow linings compared to a surface sediment(Table 12.7;Figure 12.10)(Henriksen et ai., 1983;Kristensen et ai., 1985).Assays

0Nitrate concentration (I'M)

100 200

::~:---oI '°/

E

t

/.°,.:3. 5 J /°~ /°.£ l-c °~ Ic: °~Ig.100 10

° Bioturbated

. Non-bioturbated

(a)

Denitrification activity (nmol N cm -, d-')300 0 100 200 300

I o,.~'/° -----.°........--.

0I 0

/ I/°_°

/°-

(b)

Figure 12.9. (a) Porewater nitrate concentration and (b) denitrification activitywith depth in sediment from Norsminde Fjord, Denmark. Closed symbols arewithout infauna; open symbols represent sediment with populations of Nereis spp.,CorophiumvoiutatorandMya arenaria. (AfterS~rensen,1978.)


Table 12.7. Potential nitrification in burrow walls and faecal pellets of five infaunalspecies together with potential rates from ambient and surface sediment. Nitrification wasdetermined in aerobic slurries with surplus ammonium. Denitrification was determined inanaerobic slurries with surplus nitrate

a Kristensen et al. (1985) at 22 °c; b Henriksen et al. (1983) at 22°C; C Sayama and Kurihara(1984) at :'O°c.

of potential activity, where the conditions are optimized (surplus ammonium andoxygen),only reflect the state of microbial populations, i.e.enzyme content of thesediment, but not the actual rates and thereby the magnitude of in situnitrification. Bulk in situ rates are generally much lower than potential rates, e.g.10% (Hansen et aI., 1981). Aller et af. (1983) estimated the proportion ofammonium flux which is nitrified in burrows of the polychaete Onuphisjenneri tobe 20-50%, similar to that observed for surface sediments, 33-63% (Billen, 1978;Fenchel and Blackburn, 1979). This fraction is, however, highly sensitive tovariations in parameters like sedimentation rate, temperature and oxygenavailability. The high potential for nitrification in burrow walls correlates withthe content of mucus and fine particles (Table 12.2; Figures 12.3 and 12.10).Despite their chemoautotrophic metabolism, nitrifiers are commonly associatedwith the fine-particle and high-organic fraction of sediments. It has beensuggested that this apparent correlation is due to the pH-buffering capacity ofsuch particles retaining an optimum pH for nitrifiers (Fenchel and Blackburn,1979).Higher availability of ammonium in the high-organic fraction of the wallmay also be a possible mechanism (Henriksen et af., 1983).By relating measuredpotential nitrification rate to predicted oxygen penetration into surface andburrow wall sediment, Kristensen et a1. (1985) estimated that nitrification inburrows of a natural population of Nereis virens account for 10-70% (average40%) of the bulk sediment nitrification. This is in accordance with Henriksenet a1.(1980),who estimated the burrow contribution for this species to be 35%,and Blackburn and Henriksen (1983),who found 18% for the polychaete Laniceconchilega.

Potential activity(nmolcm- 3 h -1)

Wall Faecal Ambient Surfacelining pellets sediment sediment

NitrificationN ereis virens' 229 - <50 90Corophium volutatorb 45 17 17Mya arenariab 50 4 19Macoma balticab - 217 10 29

DenitrificationN ereis virens' 30 - <30 60N ereis japonicac - 141 11 32


~ 15

"E 0'6Q)'"..,

~a.t3 5

0Potential rate (nmol cm-' h-1)

50 100 150 200

5

'",. 0 °

X/0 I°

10 Nitrification

.

10

I

°v.X° .

II° .

Denitrification

I

° Burrow wall

. Surface

15

Figure 12.10. Rates of potential nitrification and denitrification inradial profiles around a nereid burrow and vertical surface profilesin sediment from Norsminde Fjord, Denmark. (After Kristensenet aI., 1985.)

Denitrification in coastal marine sediments has been intensively studied (e.g.Hattori, 1983; Koike and ~rensen, this volume), but only a few reports haveexamined the quantitative aspects of infaunal burrows. The nitrate produced bynitrification in the oxic layers will either pass to the overlying water or enter theanoxic sediment where it is reduced to free nitrogen gas by denitrification, andthereby lost from the ecosystem (Vanderborght and Billen, 1975). Evidencesuggests that only 27-57% of the reduced nitrate is accounted for by denitrific-ation; the remainder is reduced to ammonium by dissimilatory pathways (Koikeand Hattori, 1978).This fraction may, however, vary according to sediment typeandredoxregime.Denitrificationisprimarilydependentupon anoxicconditions,


availability of nitrate and the presence an energy source. These conditions areapparently satisfied in the mucus-lined burrows of benthic animals, especiallyduring periods ofventilatory rest. Nevertheless, Kristensen et al. (1985)found noelevated potential activity in the walls of nereid burrows (Figure 12.10). Theyinstead found an increased activity in the oxic surface sediment, which may implythe presence of anaerobic microniches and a generally high activity of chemo-heterotrophs in this zone. No specific mechanisms are known to explain thissurprisingly low activity of denitrifiers in burrow walls. In situ denitrificationrates in the walls, however, may be of considerable magnitude. By the use of in situnitrate profiles, Kristensen et at. (1985) estimated that denitrification in nereidburrows account for 50-80% of the bulk sediment rate. Similarly, Chatarpaulet at. (1980)showed that Tubifex sp. in stream sediment account for 44% of thebulk denitrification, but a major part of the denitrifying activity is directlyassociated with the body ofthis oligochaete worm. No such association is knownfor other infaunal species.A close spatial and temporal coupling to nitrification isresponsible for the high rate of denitrification in burrows. The variable andgenerally narrow oxic zone around burrows provides a very short diffusion pathfor nitrate into the surrounding anoxic denitrification zone. Nitrate will besupplied by nitrification in the oxic burrow lining and by import duringventilation periods. The intermittent ventilation pattern is, in addition to theclose spatial coupling, responsible for a temporal coupling of the two processes.Denitrifiers can, especially during ventilatory rest periods, reduce most of the

v R v R105

0

750

(-O~

I

!0

100 f- cf>o~

i :lJ ."'""

" 0.0 I.!: 85Q)

~Z 80

10 20

Time (min)

40

Figure 12.11. An example of nitrate concentration changes in aburrow of Nereis virens. The overlying water concentration is107f.lM.V and R indicate ventilation and rest periods, respectively.(After Kristensen, 1984.)


nitrate produced in the burrows (Figure 12.11).In surface sediments, however,only 6-35% of the nitrate produced generally is consumed by denitrification(Billen, 1978;Nishio et aI., 1982).

The exchange of nitrate between the sediment and overlying water is affectedconsiderably by the burrow-dwelling infauna. In the presence of different infaunalspecies the flux of nitrate either increases or decreases. This may be attributed tosubstantial variation of the coupling and rates of nitrification and denitrificationactivity in the burrow environments (Aller this volume). Shallow burrowers, likeCorophium volutator, which have a very high ventilation activity and largeburrow volume compared to size, are usually very effective increasers ofnitrification, because oxygen generally penetrates relatively deep into the burrowwalls(Henriksenet al., 1983).The deepburrower,Nereisvirens,usuallyshowsaflux of nitrate into the burrows, suggesting a high rate of denitrification. Theconcentration in the overlying water is, however, an important determinant ofnitrate flux. The equilibrium concentration for nitrate in the burrow water (theconcentration where no nitrate flux is observed either in or out of the burrow) islow for nereids. Even at very low nitrate concentrations in the overlying water,nitrate will readily diffuse into the burrow wall to be denitrified in the anoxicparts. Kristensen (1984) found that for Nereis virens nitrate is consumed by theburrow wall at concentrations above 5-10 P.M.Below the equilibrium con-centration nitrate is released at a low rate.

12.7 FAECAL PELLETS AND MICRONICHES

Infaunal macro invertebrates not only affect the biogeochemical cycles in coastalsediments by their burrow-dwelling life habit. During feeding (i.e. deposit- orfilter-feeding) the majority of infaunal animals selectively concentrate organic-rich material into faecal pellets. For the bivalve Macoma baltica the organiccontents of faecal pellets are observed to be ~ 5 times higher than the bulkcontent of a Danish coastal sediment (Henriksen et al., 1983). It has long beenrecognized that faecal pellets are sites of high microbial activity (Newell, 1965;Fenchel, 1972; Hylleberg, 1975; Hargrave, 1976; Yingst and Rhoads, 1980).Passage of detritus particles through an invertebrate gut completely altersbacterial populations through digestion. The egested faecal pellets are rapidlyrecolonized by successions of microorganisms. Mucus-wrapped faecal micro-aggregates, relatively resistant to disintegration, are usually expelled and mixedinto the oxidized zone in surface sediments. Here they are responsible for aheterogeneous microbial distribution, producing microniches of elevated activ-ity. Decomposition measured as oxygen uptake in faecal pellets generally shows amaximum after a couple of days recolonization, followed by a time-dependentdecrease. The faecal pellets of the gastropod Littorina littorea, feeding ondecaying Laminaria, consume 1.5mg O2 g-1 h -1 after 2 days, compared to0.5mg°2 g-1 h-1 for the undigestedLamil1ariadetritus(Hargrave, 1976).


However, no quantitative measurements of ammonium mineralization in faecalpellets are known.

The high rate of microbial oxygen consumption in faecal pellets may affect thedistribution of oxygen in surface sediments. J~rgensen (1977)demonstrated thepresence of reduced microniches inside faecal pellets of 50-200 11Min diameter.This in turn promotes anaerobic processes (denitrification and sulphate reduc-tion) to take place within the oxic surface sediment. An aerobic process, such asnitrification, is affected considerably by these structures and may be responsiblefor a part of the measured oxygen uptake (Jahnke, 1985). Faecal pellets fromMacoma baltica, sampled at the sediment surface, exhibit higher rates (10-20times) of potential nitrification compared to ambient surface sediment andpseudofaeces (Table 12.7)(Henriksen et ai., 1983).This confirms that nitrifyingbacteria are associated with the silty-clay and organic matter fraction ofsediments. The microniches created by faecal pellet production may therefore bequantitatively important for bulk sediment nitrification. Recently a strongcoupling of nitrification and denitrification has been demonstrated in the oxicsurface layer of coastal sediments (Jenkins and Kemp, 1984).The strength of thiscoupling, where> 99% of the nitrate produced is subsequently reduced, suggestthat the two processes occur in close proximity to one another. The existence ofreduced microenvironments in faecal pellets may explain these observations.Sayama and Kurihara (1983)observed that faecal pellets, incubated aerobically,show a 5-10 times higher denitrifying activity than the surrounding sedi-ment (Table 12.7). The presence of anaerobic microniches is evident by thesignificantly lower rates of denitrification in crushed faecal pellets, 20 comparedto 141nmol N cm -3 h -1 in intact pellets. Anaerobic microniches may, therefore,together with the burrow structures, be active sites of nitrogen removal fromthe marine ecosystem. They apparently increase decomposition and therebyammonium production, nitrification and denitrification.

12.8 CONCLUSIONS

A variety of reports have indicated the importance of nutrient regeneration incoastal marine sediments (e.g. Nixon, 1981)and growing evidence suggests thatthe benthic fauna playa significant role in nutrient cycling. If estimates of annualprimary production are converted to a nutrient demand it becomes apparent thatthe benthic nutrient input can support a substantial part of the primaryproduction. In coastal environments benthic nitrogen regeneration has beenestimated to supply 26-101 % of the phytoplankton demand (Table 12.5).Thefaunal stimulation of mineralization processes in the upper centimetres ofsediments is responsible for removal of organic material at a rate higher thanexpected by purely microbial action (Figure 12.12). Benthic animals maytherefore increase nutrient turnover in coastal ecosystems and improve primaryproduction. This implies that an increased part of the nitrogen pool generally

- _d- -- --


Figure 12.12. A generalized net annual nitrogen budget for sediment from Danishcoastal waters (gN m - 2 Y- 1).The infauna is for simplicity composed of only onespecies; N ereis virens, with a density of700 individualsjm2. The rates are based on theknowledge of the yarious processes and are recalculated to the present purpose, Theoxic zone at the surface and burrow walls are assumed to be 5 and I mm, respectively

should be found in the water column, either as nutrients or fixed in organisms,and less should be fixed as organic detritus in the sediments.

The release of inorganic nitrogen across the sediment-water interface isgenerally lower than expected, based on the flux of phosphorus and oxygen. Theanomalously high O:N and low N:P ratio usually observed can be a result ofdenitrification occurring in the anoxic parts of the sediment. The activities ofmacrobenthos may increase both nitrification and denitrification in the sediment(Figure 12.12). Microenvironments, such as faecal pellets and intermittentlyventilated burrows, create a close spatial and temporal coupling of the twoprocesses. According to the annual nitrogen budget for a sediment system fromthe Limfjord, Denmark (700 individuals of Nereis virens/m2) shown inFigure 12.12, denitrification at the sediment surface removes about 13% of thenitrogen originally incorporated, while a total of 30% is denitrified by includingthe benthic infauna. The animals may therefore be responsible for more than halfof the bulk sediment denitrification in coastal areas. Sediments could consequent-ly act as major sinks in the marine nitrogen cycle, and be responsible for thegeneral nitrogen limitation of primary production in this environment, despitethe extensive effiux of inorganic nitrogen. However,problemswith eutrophic-

8 "30

'rt toxic10 8

NO]burrowOrg- N ;> NH

rt" 5 - 2

anoxic

N2Nf:203

;> NH+"NH+

F'/' " t +8:> Org ----7-NH"Org- N

N Nereist3

---n_-


ation in manycoastal areas show that anthropogenic nutrient inputs canoverwhelmthe capacity of the benthic communitiesand thereby disturb thenatural balance.

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benthic fauna and biogeochemical processes in marine sediments

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