Effects of bioturbation by tube-dwelling chironomid larvae on oxygen uptake and denitrification in...

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Freshwater Biology (1996) 35, 289–300

Effects of bioturbation by tube-dwelling chironomidlarvae on oxygen uptake and denitrification ineutrophic lake sediments

J O N A S M . S V E N S S O N A N D L A R S L E O N A R D S O NDepartment of Ecology/Limnology, Ecology Building, University of Lund, S-223 62 Lund, Sweden

S U M M A R Y

1. Oxygen uptake and denitrification were determined in two bioturbated sedimentsfrom a eutrophic lake in southern Sweden. In laboratory mesocosms, an organicprofundal sediment was incubated with Chironomus plumosus L. and a sandy littoralsediment with an organic-rich top layer was incubated with Polypedilum sp. Both speciesof chironomid are sediment tube-dwelling.2. Oxygen consumption, expressed per gram of larval dry weight, was enhanced to thesame extent by the larvae in both sediments. Measurements of the respiration rate ofindividual larvae revealed that the respiration per gram dry weight of the smallerPolypedilum sp. was more than three times higher than that of C. plumosus.3. Denitrification was measured using the ‘nitrogen isotope pairing’ technique. In theorganic sediment, denitrification of nitrate from the water phase (dw) and denitrificationof nitrate from coupled nitrification (dn) were each correlated with the biomass ofC. plumosus. In the sandy sediment, dw was correlated with the biomass of Polypedilumsp., while dn did not show any correlation with Polypedilum sp.4. Oxygen uptake in the organic sediment was increased by a factor of 2.5, dw 5-foldand dn 2.5-fold at a biomass of 10 g m–2 dry weight of C. plumosus. The same biomass ofPolypedilum sp. in the sandy sediment resulted in a 2-fold stimulation of oxygen uptakeand a 3-fold stimulation of dw, while dn was not affected. These differences instimulation between oxygen uptake and denitrification by the larvae in the sedimentssuggest that the stimulation pattern cannot be explained by simple extension of thesediment surface. The burrows evidently reduce the distance between the nitrate sourcein the water column and the denitrifiers in the anoxic zones.5. This study indicates that bioturbation by macrofauna elements can have a greatimpact on denitrification in lake sediments, and that different organisms can influencenitrogen turnover in specific ways.

Introduction

Since excessive nitrogen has been identified as a eutrophication of coastal areas (Mitsch, 1992; Janssonet al., 1994; Leonardson, 1994).factor limiting phytoplankton production in marine

environments (e.g. Graneli et al., 1990), intensive Streams, ponds, lakes and other wetland areas areknown to have a capacity for nitrogen retention, andresearch efforts have been initiated to limit the trans-

port of nitrogen to the sea. Hence, great attention has denitrification seems to be the most significant processfor removing nitrogen (e.g. Nichols, 1983; Lowrancebeen paid to freshwaters to investigate their potential

as nitrogen sinks, and the restoration and creation of et al., 1984; Peterjohn & Correll, 1984; Bowden, 1987;Seitzinger, 1988; Brusch & Nilsson, 1991; Fleischer,ponds and wetlands have been suggested as measures

to reduce the transport of nitrogen, and subsequent Stibe & Leonardson, 1991; Leonardson, 1994). In order

© 1996 Blackwell Science Ltd 289

290 J.M. Svensson and L. Leonardson

to optimize restoration and creation of wetland areas in chironomid biomass (Andersen, 1977; Andersen &which high nitrogen retention is possible, an improved Jensen, 1991). These authors suggested that theunderstanding of factors regulating denitrification is enhanced nitrate consumption depended on stimu-necessary. One important factor, almost neglected in lated denitrification activity. However, no direct meas-freshwater studies, is the stimulation of denitrification urements of the coupling between denitrification andcaused by benthic animals reworking the sediment in chironomid biomass in freshwater sediment have beendifferent ways (bioturbation). reported in the literature. The role of freshwater oligo-

In estuarine coastal areas, it has been shown that chaetes in sediment nitrogen metabolism has beenbottom-dwelling animals can enhance denitrification discussed in two papers. Chatarpaul, Robinson &by a factor of 2–3, depending on sediment structure Kaushik (1979) observed that additions of tubificidand the abundance and type of benthic fauna oligochaetes increased nitrate consumption in a stream(Henriksen, Hansen & Blackburn, 1980; Kristensen, sediment. In a subsequent study, Chatarpaul, RobinsonJensen & Aller, 1991; Pelegrı, Nielsen & Blackburn, & Kaushik (1980) found evidence for simultaneous1994). In particular, tube-dwelling animals like Nereis enhancement of nitrification and denitrification by 140virens (Sars) and Corophium volutator (Pallas) that con- and 80%, respectively, in the same stream sedimenttinuously irrigate their burrows have a large effect after having added tubificid oligochaetes. However,on denitrification. These animals not only create an denitrification gases (N2, N2O) were not measured,extension of the sediment surface (Kristensen, 1984), and 15N not found in the ammonium, nitrite, nitratebut their burrows also become sites of high bacterial and organic nitrogen pools in the experimental systemsnumbers and high metabolic activity compared to the was assumed to have been lost by denitrification.surrounding sediment (Aller & Yingst, 1978; In this study we demonstrate the effect of bioturb-Henriksen, Rasmussen & Jensen, 1983; Kristensen, ation by two tube-dwelling freshwater chironomid1985; Kristensen et al., 1991). Irrigation of the burrows larvae on oxygen uptake and denitrification inresults in transport of nitrate from the water column eutrophic lake sediments. Denitrification was meas-to deeper sediment. In addition, the continuous ured using the nitrogen isotope pairing methodrenewal of oxygen can also stimulate nitrification and (Nielsen, 1992).mobilize nitrate to sites for denitrification. Hence, thecoupling between oxygen and nitrogen turnover isevidently very close in marine and estuarine sediment, Materials and methodsand is mediated by bioturbating animals living at theinterface between sediment and water. Sediment and chironomid preparation

In freshwater environments, several studies haveTwo types of sediment were collected from thereported a high correlation between sediment oxygeneutrophic lake Sovdesjon in southern Sweden duringuptake and biomass or larval number of chironomidsApril 1994. Sediment (0–20 cm) was collected with an(Hargrave, 1975; Andersen, 1977; Graneli, 1979b, 1982;Ekman grab from 4 m depth and passed through aAndersen & Jensen, 1991). In most of these studies it2-mm sieve to remove invertebrates, larger detritushas been concluded that the enhancement of sedimentand algal aggregates. This sediment was of algal originoxygen uptake cannot be explained exclusively byand highly organic. The average porosity of the topchironomid respiration. This suggests that bioturb-3 cm was 94% and the organic content 36% (by dryation activity stimulates microbial mineralization inweight). At the same time, chironomids were collectedthe sediment (Andersen & Jensen, 1991). Van de Bund,from the same depth. The fauna at 4 m was dominatedGoedkoop & Johnson (1994) concluded that physicalby fourth instar Chironomus plumosus with an averagedisturbance (bioturbation) by Chironomus ripariusdry weight of 4.1 6 1.1 mg ind–1 (mean 6 SD). A sandy(Meigen) was the main factor increasing bacterialsediment was also collected from another site in theproduction about 4-fold compared with controls inlake close to the shore, at 1 m depth, and sieved instudies with surficial sediment. In freshwater, Chiron-the same way. This sediment consisted mainly of fineomus plumosus L. has also been shown to enhancesand with an organic-rich top layer about 0.5 mmnitrate consumption in the water overlying profundal

sediment, and this was correlated positively with deep. The average porosity of the top 3 cm was 25%

© 1996 Blackwell Science Ltd, Freshwater Biology, 35, 289–300

Bioturbation, oxygen uptake and denitrification 291

and the organic content 0.5% (by dry weight). The ents in the water column and that the systems werein steady state.chironomid fauna found at this site was dominated

by fourth instar Polypedilum sp. with an average dryweight of 0.52 6 0.15 mg ind.–1. Both sediments were Sediment oxygen consumptionstored without air bubbling and allowed to settle in

After another 7 days of incubation, to stabilize theopen jars (66 l) in darkness at 4 °C for 2 weeks. Thesediment–water system and to acclimatize the animalschironomid larvae were stored separately, at the sameto the sediment, oxygen consumption was measuredtemperature, with a small amount of original sedimentin the cores. From each replicate, 60 ml of water wasin small buckets containing continuously aerated lakewithdrawn 3–4 cm above the sediment surface, andwater. Chironomid larvae were hatched in the laborat-transferred to 25 ml Winkler vials. These samplesory, and identification was made on adults. The in siturepresented the initial oxygen values. After replace-nitrate concentration of lake water was c. 100 µM.ment of the withdrawn volume with aerated circulat-After 2 weeks, during which time the sedimentsing water, all cores were immediately capped, andhad settled and stabilized, thirty-two plastic cylindersincubated for 41–42 h in darkness under magnetic(25 cm long, 4.4 cm inner diameter) were pressedstirring. After the incubation period, another 60 mldown into the open jars and temporarily closed withwas withdrawn from the same depth as the initialbutyl stoppers. One by one, 7–9-cm sediment coressample, and transferred to 25-ml vials. This finalwere withdrawn and transported to buckets, and thesample was taken through a tube mounted in the capoverlying water phase was replaced with nitrate-without opening the cylinders. It was done withoutand ammonium-free artificial lake water preparedany immediate replacement of the water phase.according to Lehman (1980). The water volume aboveSamples for oxygen measurements were taken withoutthe sediment was 220 6 14 ml (mean 6 SD). Eachdisturbing the sediment surface, and no animals werecylinder was equipped with a rotating magnetic stirrerobserved to be dead at this time.

connected to the cylinder wall 5–6 cm above thesediment surface. The open cylinders were moved

Chironomid oxygen respirationto incubation chambers and placed around rotatingcentral magnets (47 r.p.m.). The stirring did not resus-

A separate experiment was conducted to measurepend the sediment. Aerated nitrogen-free artificial lake

oxygen respiration of C. plumosus and Polypedilum sp.water was continuously circulated to the incubation Groups of 0–4 C. plumosus (n 5 14) and 0–8 Polypedilumchambers at a constant flow rate of 1.3 l min–1. The sp. (n 5 12) were incubated in 25 ml Winkler vialswater 2–3 cm above the sediment–water interface was with oxygen-saturated artificial lake water (Lehman,saturated with oxygen at the start of the experiment. 1980) for 24–26 h in darkness at 10 °C. Before transfer-The temperature was held constant at 10 °C during ring the larvae to Winkler vials they were offeredthe experiment and all incubations were performed in short glass tubes as surrogate tunnels and acclimatizeddarkness. After 1 day in the incubation chamber, to 10 °C for 24 h. The glass tubes had diameters ofchironomids were added to the sediment cores. Zero, 3 mm or 1.5 mm and lengths of 20–30 mm or 10–20 mm1, 2 and four individuals of C. plumosus were added for C. plumosus and Polypedilum sp., respectively. Theto the organic sediment cores in randomly distributed glass tubes containing chironomids were then trans-replicates of four. Individuals of Polypedilum sp. were ferred to the incubation bottles with oxygen-saturatedadded to the sandy sediment cores at densities of 0, artificial lake water. Usually the C. plumosus larvae10, 20 and 40, each treatment being replicated four remained inside the glass tubes during incubation,times. The chironomids immediately dug down into while individuals of Polypedilum sp. were more reluct-the sediment. These additions correspond to in situ ant to stay inside the tubes. Instead, several individualsdensities of 0, 657, 1315 and 2630 ind. m–2 of C. of Polypedilum sp. crawled out and stayed betweenplumosus and 0, 6570, 13 500 and 26 300 ind. m–2 of the glass tube and the bottom of the Winkler vials.Polypedilum sp. Oxygen measurements were taken Since the frequency and duration of undulating bodyduring this incubation period to ensure the magnetic movements in all animals were observed to be similar,

it was assumed that animals were not stressed bystirring was sufficient to avoid vertical oxygen gradi-



being located outside the tubes. Winkler reagents were the sample water was replaced with helium. Aftervigorous shaking, 30 µl of the gas phase was injectedadded to the vials directly at the end of the incubation

period. After the respiration measurements, the total into an isotope ratio mass spectrometer (Europe Scient-ific, Crewe, U.K.). The percentage 15NO3

– enrichmentdry weight (105 °C) of all animals in each bottle wasdetermined. in the water phase was estimated by measuring the

NO3– concentration before and after the addition of

15NO3– (Nielsen, 1992).

Denitrification

After measuring the sediment oxygen consumptionCalculations

all cores were incubated for another 7 days underartificial water in the dark at 10 °C, without stoppers Oxygen uptake (mg O2 m–2 h–1) for the cores wasand subject to continuous magnetic stirring. This was calculated from the changes in oxygen concentrationto allow for stabilization and equilibration of the two measurements apart. The oxygen consumption vsediment–water processes. To acclimatize the bacterial time was assumed to be linear. No measurementspopulation to nitrate-enriched (circulating) water, were below 0.5 mg O2 l–1.K14NO3 was added to the bulk water of the reservoir Rates of denitrification m–2 were estimated by usingon the sixth day, giving a final concentration in each the 15N isotope pairing technique (Nielsen, 1992):core of 0.796 6 0.006 mg 14NO3-N l–1 (57 µM). One day

d15 5 (14N15N) 1 2(15N15N) (Koike & Hattori, 1978)later the incubation for the denitrification measure-ments was carried out. K15NO3 (99%) was added to the d14 5 [d15(14N15N)]/2(15N15N)water phase in each core to give a final concentration of

The production of single-labelled (14N15N) and double-2.92 mg NO3-N l–1 (208 µM, 73% 15NO3). The cores

labelled (15N15N) dinitrogen pairs represents the netwere capped and incubated in darkness for between

fluxes and is used to calculate d15 and d14 which are3 and 4.25 h. The incubation period was set to ensure

the rates of denitrification of 15NO3– and 14NO3

–,a maximum oxygen depletion of 20%. At the end of

respectively. The rate of denitrification of nitrate diffus-the incubation the caps were removed and water

ing from the overlying water (dw) was calculatedand sediment were gently mixed with a 30 cm long

from d15 and %15NO3–, where %15NO3

– is the 15Nstainless steel forceps. Samples of the slurry were

atom% of the reservoir water:transferred to and stored in 12 ml gas-tight glass

dw 5 d15/%15NO3–containers containing 2% ZnCl (50% saturation) to

stop further microbial activity. All containers were The rate of denitrification of nitrate produced bystored for c. 1 month at 4 °C until analysis. Directly nitrification (coupled nitrification–denitrification) wasafter the denitrification sampling, the remaining slurry calculated by the difference:samples were sieved, and the total dry weight (105 °C)

dn 5 (d15 1 d14) – dw (Nielsen, 1992)of all chironomids in each core was determined. Theaverage mortality of C. plumosus and Polypedilum sp. The sum of dw and dn represents the total denitrifica-was 15% (range 0–50%) and 22% (range 0–55%), tion measured in the core.respectively.

ResultsAnalysis

Oxygen uptakeDissolved oxygen concentrations were derived fromWinkler titrations using an automatic potentiometric The oxygen consumption in both types of sediment

was significantly enhanced by an increased biomasstitrator (Mettler TM DL21) with high precision (0.1–0.3% coefficient of variance; Graneli & Graneli, 1991). of chironomids (Fig. 1a,b). Oxygen consumption in the

organic sediment with C. plumosus was only slightlyThe 12-ml slurry samples for denitrification studieswere sent to DMU, Silkeborg, Denmark, and analysed higher than in the sandy sediment with Polypedilum

sp., i.e. 1.42 and 1.22 mg O2 g DW–1 h–1 (regressionfor 15N-labelled dinitrogen pairs (14N15N and 15N15N)formed by denitrification (Nielsen, 1992). Four ml of coefficients in Fig. 1a and b), respectively (P . 0.05;



Fig. 2 Macrofaunal oxygen consumption in experiments inbottles. (a) Chironomus plumosus (rs 5 0.90, P , 0.05) and

Fig. 1 Oxygen consumption rates (6 SD, n 5 4) at 10 °C in(b) Polypedilum sp. (rs 5 0.77, P , 0.05) in relation to larval dry

(a) organic sediment with different densities of Chironomusweight. Fitted lines are based on simple linear regression and

plumosus (rs 5 0.85, P , 0.05) and (b) sandy sediment withSpearman rank coefficients of correlation are shown (n 5 16).

different densities of Polypedilum sp. (rs 5 0.96, P , 0.05). Bothsediments from Lake Sovdesjon. Fitted lines are based onsimple linear regression and Spearman rank coefficients of

Fig. 2b). The increase in O2 consumption rate withcorrelation are shown (n 5 16).increasing larval biomass was greater than the meas-ured increase in O2 uptake in sandy sediment with

Student’s t-test, comparing simple linear regression added Polypedilum sp.equations; Zar, 1974). Control values (0 chironomids)for the organic sediment were somewhat lower than

Denitrificationfor the sandy sediment (P . 0.05; ANOVA), 10.9 and12.7 mg O2 m–2 h–1 (intercept values on y-axis in Fig. 1a Data calculated from the average of dn and dw (n 5

and b), respectively. 4) in cores with no chironomids show that the rate ofThe chironomid oxygen respiration experiments denitrification of nitrate supplied by nitrification (dn)

(Fig. 2a,b) revealed that C. plumosus consumed was low compared with the denitrification activity0.59 mg O2 g DW–1 h–1 (regression coefficient in based on nitrate diffusing from the overlying waterFig. 2a) which means that 42% of the oxygen consump- (dw; Figs 3a,b and 4a,b). In the organic sediment dntion in sediment (see above) was due to the larvae. corresponded to 14% of the total denitrification, whileThe smaller Polypedilum sp. collected in the sandy in the sandy sediment dn made up only 5% of thesediment had an O2 consumption rate more than three total denitrification. In the organic sediment the denit-times that of the C. plumosus larvae, i.e. rification rate showed a clear relationship to the bio-

mass of chironomids (Figs 3a and 4a). Both1.88 mg O2 g DW–1 h–1 (regression coefficient in



Fig. 4 Denitrification rates of nitrate from coupled nitrification,Fig. 3 Denitrification rates of nitrate from the overlying water,dn, at 10 °C in (a) organic and (b) sandy sediment from Lakedw, at 10 °C in (a) organic and (b) sandy sediment from LakeSovdesjon in relation to larval dry weight of ChironomusSovdesjon in relation to larval dry weight of Chironomusplumosus (rs 5 0.84, P , 0.05) and Polypedilum sp. (rs 5 0.09,plumosus (rs 5 0.85, P , 0.05) and Polypedilum sp. (rs 5 0.85,NS), respectively. Fitted lines are based on simple linearP , 0.05), respectively. Fitted lines are based on simple linearregression and Spearman rank coefficients of correlation areregression and Spearman rank coefficients of correlation areshown (n 5 16).shown (n 5 16).

and dn 2.5-fold. In the sandy sediment the stimulationdenitrification of nitrate originating from the overlying

of oxygen uptake was 2-fold, for dw about 3-foldwater (Fig. 3a) and denitrification of nitrate coming

while dn was not significantly affected by 10 g DW m–from nitrification (Fig. 4a) were linearly correlated 2 of Polypedilum sp.with the biomass of C. plumosus. In the sandy sediment,dw was clearly correlated with the biomass of Polypedi-

Discussionlum sp. (Fig. 3b), but dn did not show such a relation-ship (Fig. 4b).

Oxygen uptakeIn conclusion, oxygen uptake rate was stimulated

(based on the mean value at 0 g DW m–2) by the A comparison of the total oxygen uptake of the organicsediment with added C. plumosus (Fig. 1a) and thechironomids to approximately the same extent in both

sediments (Fig. 5a,b), while there was a difference oxygen respiration of C. plumosus (Fig. 2a) revealedthat the total oxygen uptake was higher than couldbetween the sediments regarding the stimulation in

denitrification (dw and dn). Thus, in the organic be accounted for by larval respiration alone. The ratiobetween the slopes of the two regression lines (thesediment with 10 g DW m–2 of C. plumosus, the oxygen

consumption was stimulated 2.5-fold, dw about 5-fold sediment oxygen uptake v macrofauna dry weight



chironomid burrows evidently creates favourable con-ditions for bacteria associated with the tube walls(van de Bund et al., 1994). Local effects on bacterialproduction can be strong when this active irrigationtransports oxygen and nutrients to deeper sedimentlayers.

The experiments with Polypedilum sp. revealedanother pattern. The high individual oxygen con-sumption of the larvae was equivalent to more than100% of the enhancement of total sediment oxygendemand in the sandy sediment. Thus, the larvaeseem to consume all the available oxygen that hadbeen diffused or transported to the sediment, leavingno oxygen for bacterial respiration or nitrification.

The distribution of the enhanced oxygen consump-tion of the sediments containing C. plumosus larvaeis illustrated by considering absolute oxygen figuresfor chironomid additions of 10 g DW m–2. The totalenhancement in oxygen uptake of the organicsediment was 14.2 mg O2 m–2 h–1, of which thechironomids alone consumed 5.9 mg O2 m–2 h–1.Based on stoichiometric calculations of ammoniumoxidation to nitrate, it was estimated that theenhanced dn required only 0.97 mg O2 m–2 h–1.Hence, most of the enhanced oxygen consumption,

Fig. 5 Relative rates of oxygen consumption, denitrification of 7.33 mg O2 m–2 h–1, was consumed by the stimulatednitrate from the overlying water (dw) and denitrification of respiratory activity of the microbial population asnitrate from coupled nitrification (dn) at 10 °C in (a) organic

well as increased oxidation of inorganic chemicaland (b) sandy sediment from Lake Sovdesjon in relation tospecies in the burrows and the sediment. Thelarval dry weight of Chironomus plumosus and Polypedilum sp.,

respectively. A relative rate of 1 represents cores free of addition of Polypedilum sp. to the sandy sedimentmacrofauna. resulted in a similar enhancement in oxygen uptake,

i.e. 12.2 mg O2 m–2 h–1. According to our experimentsthe oxygen requirement of this species alone exceededand C. plumosus respiration v macrofauna dry weight)

was 2.4 for the organic sediment. In experiments with the increased oxygen consumption of the sedimentcontaining Polypedilum larvae. This agreed with theC. plumosus, Graneli (1979b) found a ratio of 3.2 in a

similar restratified organic sediment from the result that no statistically significant increase wasfound in the coupled nitrification–denitrificationeutrophic lake Vombsjon (in close proximity to Lake

Sovdesjon). The data of Andersen (1977) for a profun- activity in this sediment. The chironomids wereprobably responsible for the total increase in oxygendal organic sediment from Lake Langso, Denmark,

give a quotient of c. 1.6, which also compares with consumption, and none of the increase was due toincreased nitrification and bacterial respiratory activ-our ratio of 2.4. Graneli’s slopes of regression for

C. plumosus respiration (0.56–0.77) were also similar ity in this sediment.There was a significant difference between theto our value (0.59). At a dry weight of 10 g m–2, the

effect of C. plumosus on total sediment oxygen uptake individual oxygen respiration of C. plumosus andPolypedilum sp. The latter species was collected in acorresponds to an enhancement of 42% compared with

cores without chironomids. This indicates that the sandy littoral sediment at a water depth of 0.5–1 m,and was shown to respire three times as muchremaining 58% of the enhancement must be due to

increased bacterial respiration within or close to the oxygen per gram biomass as C. plumosus underidentical conditions (Fig. 2). This result is not surpris-larval burrows. The active pumping of water through



ing. Because small animals have high ratios of body 200 000 m–2 (Polypedilum pavidus Hutton; Forsyth &McCallum, 1983) have been reported.surface to body volume, they generally have higher

metabolic rates and therefore greater energy require-ments per unit of body weight than larger animals Denitrification(Pianka, 1978). Polypedilum sp. not only had a

The nitrogen–isotope pairing method (Nielsen, 1992)higher respiration rate, they should also have beenis a further development of the analysis of the mixingphysiologically adapted to the higher and lessof 15NO3 and 14NO3 in studies of soil denitrificationvariable oxygen concentrations characteristic of theintroduced by Hauck, Melsted & Yankwich (1958).shallow part of the lake. Chironomid species livingIt is assumed that 15NO3 does not interfere within the profundal zone of eutrophic lakes are probablydenitrification of 14NO3, and that there exists a uniformbetter adapted to low oxygen concentrations thanmixing of added 15NO3 with the naturally occurringspecies predominantly from well-oxygenated habitats14NO3 (Nielsen, 1992). Bioturbation by benthic fauna(Heinis, Sweerts & Loopik, 1994). Hence, C. plumosus,allows uniform mixing since 15NO3 mixes randomlyliving in the profundal zone, have a lower oxygenwith 14NO3 in the aerobic zone surrounding thedemand compared to Polypedilum sp., living in theanimals before the 15NO3 reaches anaerobic sites andlittoral zone of the lake. From the studies of Berg,is denitrified. Hence, the method has been used suc-Jonasson & Ockelmann (1962) and Hamburger, Dallcessfully in bioturbated and non-bioturbated estuarine& Lindegaard (1994) it is also known that larvae ofsediment with additions of up to 330 µM 15NO3 (Pelegrıthe same species can have varying oxygen demandset al., 1994; Pelegrı & Blackburn, 1995).depending on where they occur. Jonasson (1972)

At a biomass of 10 g C. plumosus m–2 in the organicshowed that under identical temperature and oxygensediment there was a 5-fold stimulation of denitrifica-conditions C. anthracinus Zetterstedt captured fromtion of nitrate from the water phase (dw) and athe oxygen-rich sublittoral zone of Lake Esrom,2.5-fold stimulation of oxygen consumption and

Denmark, had a higher oxygen consumption ratedenitrification of nitrate from nitrification (dn). This

than larvae of the same species that were collecteddifference in enhancement shows that extension of the

from the oxygen-poor profundal zone. This wassediment surface alone cannot explain the stimulation

explained by a fundamental difference in physiologypattern, since this should stimulate all processes to

between the larvae, and this might also explain thethe same extent.

large difference in oxygen consumption rates between The oxic layer of the burrow walls and adjacentC. plumosus and Polypedilum sp. in our study. A sediment is significantly thinner than that of thebehavioural adaptation strategy of chironomid larvae sediment surface (Jorgensen & Revsbech, 1985). Thisto decreasing oxygen pressure in deep water also is probably caused by higher bacterial activity closeincludes increasing the water and oxygen flow to the burrow walls. In addition, this is also a physicalthrough their burrows (Leuchs, 1986; Heinis & phenomenon dependent on the radial diffusion geo-Crommentuijn, 1992). Unfortunately, we could not metry which the burrows provide (Aller, 1982). As afind any published data on the respiration rate of consequence the burrows create a shorter pathway forPolypedilum sp. nitrate to diffuse into anaerobic sites in the sediment

The numbers of chironomids added to the sedi- compared with the thicker oxygen barrier at the sedi-ments in this study (0–2630 C. plumosus m–2 and 0– ment surface. Hence the bioturbation of chironomids26 300 Polypedilum sp. m–2) were within the range would increase denitrification of nitrate originatingnormally found in eutrophic lakes. Abundances from from the lake bottom water (dw). The width of the200 to several thousand chironomids m–2 of C. diffusion barrier depends on the extent to whichplumosus type are reported from the profundal oxygen can penetrate into the burrow linings. Thesediment in lakes of varying trophic states limited volume inside burrows of Nereis virens in(Thienemann, 1954). Data on the littoral taxon estuarine sediment allows aerobic conditions to lastPolypedilum sp. are more sparse. However, abund- only a short distance after which anoxic conditionsances from a few thousand m–2 (Polypedilum sp.; will prevail (Kristensen et al., 1991). The oxygen

dynamics also depend on the ventilation pattern ofvan de Bund & Groenendijk, 1994) to almost



the organism, which in turn is dependent on the was not the case. Instead dw was stimulated to asomewhat greater extent in the organic sediment thanoverall oxygen conditions in the water overlying the

sediment. In sediments rich in organic material the in the sandy sediment. Both C. plumosus and Poly-pedilum sp. create tunnels and burrows, but in theoxygen diffusing into the walls will be consumed very

fast, and the length of the nitrate diffusion pathways incubated sediment cores it was observed that thelatter do not penetrate the sediment by more thanto anoxic sites will be reduced.

The inevitable consequence of the addition of chiron- c. 2 cm while C. plumosus penetrate down to 7–9 cm.Hence, Polypedilum sp. only circulate bottom water inomids to the sediment cores is an increase of organic

matter and the potential influence this should have the upper 2 cm of sediment at most, while C. plumosuspump water through a much larger volume of sedi-on the sediment processes. As long as the larvae are

alive the body content of carbon will not be available ment. Nitrate from water at the sediment surfacetherefore had a longer residence time within thefor denitrification or related processes. On the other

hand, if larvae die and decompose, they can possibly organic sediment compared with that within the sandysediment with Polypedilum sp. A longer residence timecontribute to heterotrophic processes as a carbon

source. However, in all cores where there were cases in the sediment provides a better possibility for nitrateto diffuse into anoxic sites and hence a larger stimula-of death the denitrification activity was always lower

compared with identical cores with no larval death, tion of denitrification. Another explanation of thelower stimulation of dw in the sandy sediment mightwhich could suggest that loss of an individual larva

had a negative effect on denitrification. It is more be a lack of electron donors in the deeper layers,reflected by the low organic content of this sediment.likely, though, that larval excretion products stimulate

denitrification, but it seems unlikely that there should The top 3 cm of the sediment contained 0.5% organicmaterial, but most of this was concentrated in thebe a lack of electron donors in a highly organic

sediment like the one from Lake Sovdesjon. On the uppermost 1 mm.This study confirms that bioturbation by tube-dwell-other hand, in the deeper part of the littoral sandy

sediment, larval excretion may act as an important ing macrofauna can have a large impact on denitrifica-tion in eutrophic lake sediments, but that differentcarbon source, though this was not tested in our

study. Dead and decomposed larvae can obviously organisms in different lake sediments affect the nitro-gen turnover in specific ways. Bioturbation by chirono-not explain the large enhancement of dw, either in the

organic or the sandy sediment. Excretion products mids can be an important factor for the overall nitrogenretention in lakes, ponds and other wetlands, especi-might explain some of the enhancement of dw in

the sandy sediment but hardly in the organic. The ally when high biomass of chironomids coincides withhigh concentrations of nitrate in the lake water (i.e.stimulatory effects of dw in both sediments are most

certainly an effect of the animal ventilating activity, during winter and spring). Natural environmentalconditions affecting the abundance and biomass oftransporting nitrate from the water phase to anaerobic

sediment layers. chironomid larvae (cf. Jonasson, 1972) may cause highvariability in overall nitrogen removal, both seasonallyDenitrification of nitrate diffusing from the sites

of nitrification (dn) was positively correlated with and between years. Chironomid larvae make up alarge proportion of the diet of many fish species, likeC. plumosus biomass in the organic sediment. No

similar correlation was found for dn in the sandy perch (Perca fluviatilis L.; Persson, 1983a), roach (Rutilusrutilus L.; Persson, 1983b), bream and eel (Abramissediment with Polypedilum sp. A possible explanation

is that the high respiration rate of the individual larvae brama L. and Anguilla anguilla L.; Lammens et al., 1985).Large populations of these fish can have a significantof Polypedilum sp. did not leave any excess oxygen to

diffuse into the burrow linings. This in turn prevented negative impact on populations of large benthicchironomid larvae (Persson, 1983a,b; Lammensthe development of extended oxic zones along the

burrow walls. Hence, very low nitrification can occur et al., 1985), which would diminish the totalchironomid bioturbation activity and reduce nitrogenin the sediment, and no enhancement in dn can be

expected under these circumstances. On the other removal. Most probably these effects are more pro-nounced in the profundal zone of lakes, whereas inhand, we expected a greater stimulation of dw due to

the presumed lack of oxygen in the burrows, but this the littoral zone complex interactions between habitat



in lake sediments. Interaction Between Sediment andheterogeneity, fish predators, intermediate macro-Fresh-water (ed. H.L Golterman), pp. 216–226. Dr W.invertebrate consumers and macroinvertebrate prey,Junk, The Hague.e.g. chironomid larvae, seem to have a stabilizing

Berg K., Jonasson P.M. & Ockelmann K.W. (1962) Theinfluence on chironomid abundance (Diehl, 1992).respiration of some animals from the profundal zoneeHence, manipulation of fish communities in lakes, e.g.of a lake. Hydrobiologia, 19, 1–40.large-scale reduction of cyprinid populations in order

Bowden W.B. (1987) The biogeochemistry of nitrogen into restore eutrophic lake ecosystems (cf. Jeppesenfreshwater wetlands. Biogeochemistry, 4, 313–348.

et al., 1990a,b; Riemann et al., 1990; Hamrin, 1993), isBrusch W. & Nilsson B. (1991) Nitrate transformation

expected to result in increased profundal chironomid and water movement in a wetland area. Nitrogen andbiomass, and enhanced nitrogen turnover and reten- phosphorus in fresh and marine waters. Project abstractstion. However, Jeppesen et al. (1990a,b) and Hamrin of the Danish NPo research programme, Miljøstyrelsen,(1993) do not report any macroinvertebrate studies, Copenhagen.while Riemann et al. (1990) found no statistically signi- Chatarpaul L., Robinson J.B. & Kaushik N.K. (1979) Roleficant effect on the chironomid populations 2 years of tubificid worms on nitrogen transformations inafter the manipulation. Plans to create and restore stream sediment. Journal of the Fisheries Research Board

of Canada, 36, 673–678.ponds and wetlands in order to remove nitrogen alsoChatarpaul L., Robinson J.B. & Kaushik N.K. (1980) Effectsmust take into account the negative effect that stocking

of tubificid worms on denitrification and nitrification inof fish can have on chironomid larval abundance andstream sediment. Canadian Journal of Fisheries andbiomass, and potentially also on nitrogen removal.Aquatic Sciences, 37, 656–663.Therefore, the objective of nitrogen removal cannot be

Diehl S. (1992) Fish predation and benthic communitysuccessfully combined with the objective of creatingstructure: the role of omnivory and habitat complexity.areas for angling or fish production.Ecology, 73, 1646–1661.

Fleischer S., Stibe L. & Leonardson L. (1991) Restorationof wetlands as a means of reducing nitrogen transportAcknowledgmentsto coastal waters. Ambio, 20, 271–272.

Forsyth D.J. & McCallum I.D. (1983) Seasonal distributionThanks to Dr Lars Sawedahl for identifying the chiron-of Polypedilum pavidus (Chironomidae: Diptera) in aomid larvae and to the Swedish Environmental Protec-eutrophic lake in New Zealand. Archiv fur Hydrobiologie,tion Agency who supported the work by grant no.97, 134–142.13311 to the second author. We also thank Lars Peter

Graneli E., Wallstrom K., Larsson U., Graneli W. &Nielsen and Søren Rysgaard for valuable technicalElmgren R. (1990) Nutrient limitation of primary

advice and for assisting with the analysis of our 15Nproduction in the Baltic Sea area. Ambio, 19, 142–151.

samples at the laboratories in Aarhus and Silkeborg.Graneli W. (1979a) The influence of Chironomus plumosus

larvae on the exchange of dissolved substances betweensediment and water. Hydrobiologia, 66, 149–159.

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