high organic carbon export precludes eutrophication responses in experimental rocky shore...

High Organic Carbon ExportPrecludes Eutrophication Responses

in Experimental Rocky ShoreCommunities

Cristina Barron,1* Nuria Marba,1 Carlos M. Duarte,1 Morten F. Pedersen,2

Cecilia Lindblad,3 Kees Kersting,4 Frithof Moy,5 and Tor Bokn6

1IMEDEA (CSIC-UIB), Instituto Mediterraneo de Estudios Avanzados, C/ Miquel Marques 21, 07190 Esporles (Islas Baleares),Spain; 2Department of Life Sciences and Chemistry, 18.1 Roskilde University, P.O. Box 260, DK-4000 Roskilde, Denmark;

3Department of Botany, Stockholm University, S-10691 Stockholm, Sweden; 4ALTERRA, Marine and Coastal Zone ResearchTeam, P.O. Box 167, 1790 AD Den Burg (Texel), The Netherlands; 5Norwegian Institute for Water Research (NIVA), Branch Office

South, Televeien 3, N-4879 Grimstad, Norway; and 6Norwegian Institute for Water Research (NIVA), Brekkeveien 19,P.O. Box 173, Kjelsaas, N-0411 Oslo, Norway

ABSTRACTWe studied the effect of nutrient inputs on the carbon(C) budget of rocky shore communities using a set ofeight large experimental mesocosms. The mesocosmsreceived a range of inorganic nitrogen (N) and phos-phorus (P) additions, at an N:P ratio of 16. Theseadditions were designed to elevate the backgroundconcentration, relative to that in eutrophic Oslofjord(Norway) waters, by 1, 2, 4, 8, 16, 32 �mol dissolvedinorganic nitrogen (DIN)l�1 (and the corresponding Pincrease). Two unamended mesocosms were used ascontrols. The nutrients were added continuously for27 months before gross primary production (GPP),respiration (R), net community production (NCP),and dissolved organic carbon (DOC) production wereassessed for the dominant algal species (Fucus serratus)and for the whole experimental ecosystem. Inputsand outputs of DOC and particulate organic carbon(POC) from the mesocosms were also quantified. TheF. serratus communities were generally autotrophic(average P/R ratio � 1.33 � 0.12), with the GPPindependent of the nutrient inputs to the mesocosms,

and maintained a high net DOC production duringboth day (0.026 � 0.008 g C m�2 h�1) and night(0.015 � 0.004 g C m�2 h�1). All the experimentalrocky shore ecosystems were autotrophic (P/R ratio �2.04 � 0.28), and neither macroalgal biomass norproduction varied significantly with increasing nutri-ent inputs. Most of the excess production from theseautotrophic ecosystems was exported from the sys-tems as DOC, which accounted for 69% and 58% ofthe NCP of the dominant community and the exper-imental ecosystem, respectively, the rest being lost asPOC. High DOC release and subsequent export fromthe highly energetic environments occupied by rockyshore communities may prevent the development ofeutrophication symptoms and render these commu-nities resistant to eutrophication.

Key words: dissolved organic carbon; Fucus serra-tus; rocky shore communities; carbon export; eu-trophication.

INTRODUCTION

Major increases in nutrient loading have promptedthe development of eutrophication symptoms in

coastal waters (Nixon 1995). Although the researcheffort to examine the causes and consequences ofcoastal eutrophication is intensifying (Vidal andothers 1999), its development has been unbal-anced, particularly in terms of research foci. Theresponse of planktonic and shallow estuarine com-munities to increased nutrient loading is relatively

Received 10 October 2001; accepted 18 July 2002.*Corresponding author; e-mail: [email protected]

Ecosystems (2003) 6: 144–153DOI: 10.1007/s10021-002-0402-3 ECOSYSTEMS

© 2003 Springer-Verlag

144

well understood (see, for example, Duarte 1995;Borum 1996; Borum and Sand-Jensen 1996), and anumber of studies have also been done on theresponses of seagrass communities to eutrophica-tion (see, for example, Duarte 1995; Hemminga andDuarte 2000). However, the responses of rockyshore communities, which are ubiquitous compo-nents of coastal ecosystems, have received little at-tention. Macroalgal blooms have been reported inassociation with increased nutrient inputs in estu-arine environments and soft sediments (Valiela andothers 1997), but not in temperate rocky shoreenvironments.

Conventional wisdom would predict a shift inrocky shore algal community structure from slow-growing macroalgae to fast-growing opportunisticalgae with increasing nutrient inputs. Although thechanges that occur in response to increased nutri-ent inputs should lead to increased specific produc-tion or a higher growth rate for the algae (for ex-ample, see Duarte 1995; Valiela and others 1997),community primary production and biomass mayremain unchanged or even decrease (Duarte 1995;Borum 1996). This situation may arise if slow-growing algae, which typically store a large fractionof their production as biomass, are replaced by fast-growing ones whose production is much higher.Hence, an increase in specific primary productionmay not suffice to lead to increased biomass if or-ganic matter remineralization, via respiration, in-creases in parallel, as would be expected from ageneral coupling between production and respira-tion in aquatic ecosystems (Duarte and Agustı1998). Changes in the community metabolism ofrocky shore communities may therefore affect theirresponse to increased nutrient inputs.

Rocky shore communities are typically autotro-phic and produce an excess of organic matter rela-tive to that remineralized in the community (Gat-tuso and others 1998). The excess organic matterproduced should lead to either increased biomass,increased sediment accumulation, and/or increasedorganic matter export. Retention of organic matterthrough sedimentation is necessarily low in rockyshore communities, which are typically exposed towaves and tidal currents (Leigh and others 1987),which leads, in turn, to high carbon export frommacroalgal communities (Duarte and Cebrian1996). Hence, excess organic matter productionmust result in either increased community biomassand/or increased export from the community. Fu-coids and kelps, which are often dominant in rockyshore communities, release a significant fraction oftheir production as dissolved organic carbon (DOC)and particulate detritus, which may be exported out

of the system in the energetic environments theyinhabit (Mann 2000).

There have been few experimental analyses ofthe response of rocky shore communities to in-creased nutrient inputs. There is, therefore, a needto experimentally test the predicted responses ofrocky shore communities to increased nutrient in-puts. Here we used a carbon mass balance approachto examine the response of the community metab-olism and carbon budget of experimental rockyshore communities to increased nutrient inputs. Inparticular, we examined the production of the ex-perimental communities and the fate of this pro-duction: biomass accretion (or erosion), respiration,and the export of particulate and dissolved organicmatter. We specifically tested the hypothesis thathigh export rates may account for the apparent lackof response of experimental rocky shore communi-ties to increased nutrient inputs.

METHODS

Experimental Setup and Design

The experiments were conducted in eight concretemesocosms (4.7 m long, 3.65 m wide, 1.35 m deep)at the Solbergstrand Marine Research Station (theOslofjord, Norway) (Bokn and others 2001). Themesocosms received water from one m depth,which flowed through the mesocosms at an averagerate of 5 m3 h�1. Tides (mesocosm volume at lowand high tide 6.25 m3 and 11.65 m3, respectively,with a tidal period of 12.3 h) and waves weresimulated in the mesocosms. Littoral communitieswere established by transferring small boulderswith associated macroalgae and fauna from the Os-lofjord into the mesocosms 2 years before thisstudy. Fucus serratus was the dominant species in allmesocosms at the time of the experiments. Fucusserratus comprised 82% of the biomass; whereas13.5% and 4.3% of the average biomass was com-prised by red and green algae. The communitystructure at the time of the study was similar to thelong-term average composition and fluctuated littleduring the study (Bokn and others forthcoming).The design and operation of the mesocosms at-tempted to reproduce the conditions in a rockyshore ecosystem. However, some processes, such asthe tides, were difficult to fully mimic, althoughthere was indeed a tidal period imposed on thewater level. The water mass was fully exchangedduring the tides, precluding the return of the samewater mass with the tide that may occur in tidalsystems.

Nutrients, such as NH4NO3 and H3PO4 (N:P 16:

Carbon Export From Experimental Rocky Shore Ecosystems 145

1), were added continuously to six basins to obtaintarget concentrations elevated by 1, 2, 4, 8, 16, and32 �mol DIN l�1 above the background dissolvedinorganic nitrogen (DIN) concentration (that is, Os-lofjord water). These concentrations were main-tained throughout the experiment. Two other me-socosms were kept as controls; they received noadditional nutrient inputs. Nutrient addition wasundertaken for 27 months prior to the initiation ofthe experiment. Nutrient concentrations in watersentering from the fjord and in outlets from thedifferent basins were measured on weekly-pooledsamples of samples collected daily (Bokn and others2001). The Oslofjord waters had elevated nutrientconcentrations, averaging 10.6 �mol DIN l�1 and0.33 �mol P l�1 over a year (Bokn and others2001). Only the mesocosms receiving nitrogen (N)inputs to elevate their N concentration by 2 �molDIN l�1 or higher exhibited concentrations signifi-cantly above those in the fjord waters for bothnitrogen (N) and phosphorus (P) (Bokn and others2001). Nutrient uptake in the mesocosms resultedin a decline of about 10% in nutrient concentra-tions in the basins relative to the input concentra-tion (Bokn and others 2001). Estimates of the totalmacroalgal cover in each of the mesocosms weremade by combining estimates of cover in the entirebasin with estimates of areal biomass derived fromharvesting of small quadrats in each cover compo-nent, for a total of seven seasonal campaigns. Fur-ther details on the experimental setup and opera-tion are provided in Bokn and others (2001, 2002).

Organic Carbon Budget

Examination of the organic carbon inputs and out-puts described below was conducted in August2000, 27 months after the initiation of nutrientadditions. In particular, we examined processes(community metabolism and net DOC release) atthe community level using bell chambers enclosingparts of the community, as well as the whole sys-tem, where measurements of particulate organiccarbon (POC) (micro- and macroscopic) and DOCinputs and outputs allowed calculation of net gainsor losses of organic carbon. For each mesocosm, wealso calculated the net rate of biomass change fromthe slopes of linear regressions between the mac-roalgal biomass and time since the nutrient inputswere initiated. Community metabolism and the netrate of biomass change were investigated in all me-socosms, whereas the net DOC production of mac-roalgal communities was examined in all meso-cosms receiving nutrient inputs and one of thecontrol mesocosms. Whole-system DOC productionwas examined in three of the mesocosms, including

one control and two moderately fertilized meso-cosms. Rates measured in oxygen units (productionand respiration) were converted to carbon units byassuming photosynthetic and respiratory quotientsof 1.

Community Organic Carbon Budget

The metabolic rate of the communities and netDOC production were measured by enclosing thedominant Fucus serratus community in chambersunder natural light conditions. The chambers con-sisted of a PVC ring (18-cm diameter) attached tothe substrate using underwater cement and closedby a polyethylene plastic bag fitted with a samplingport. Four or five replicate chambers were set ineach of seven mesocosms (one control and all of theenriched mesocosms). The Fucus communities in-cubated were chosen from the bottom or from thefourth step of the mesocosms (compare the meso-cosm design in Bokn and others 2001). The positionof the chamber did not, however, affect their pri-mary production as the macroalgae were underlight-saturated conditions (M. F. Pedersen unpub-lished).

The chambers were sampled at the onset of theincubations in the early morning, just before sunset(about 21:00 Pm), after sunrise (about 5:00 Am),and after 24 h. The full set of measurements wasconducted within 3 consecutive days. Changes indissolved oxygen concentrations during the incuba-tion period were used to estimate the gross primaryproduction (GPP), net community production(NCP), and community respiration (R). Water sam-ples from the incubations were taken with a 50-mlsyringe to estimate the dissolved oxygen concentra-tion and analyzed with a spectrophotometric adap-tation of the Winkler method, where the color ofthe I3

�-I2 couple formed during the Winkler proce-dure was measured at 430 nm and used to estimatethe concentration of oxygen from a calibrationcurve constructed against estimates derived fromWinkler titrations (Pai and others 1993; Roland andothers 1999).

R was estimated from the changes in oxygenconcentration between dawn and dusk. NCP wasestimated from the rate of change in oxygen con-centration during the full 24-h period. Finally, GPPwas estimated as the sum of NCP and R. The esti-mates were corrected for oxygen diffusion acrossthe plastic chambers, using an experimentally de-termined diffusion coefficient and the concentra-tion gradient along the experiments. The oxygenconcentration in the waters was measured in eachmesocosm with an oxygen probe and recorded as15-min averages. Macroalgal community turnover

146 C. Barron and others

rate (P/B ratios) were calculated as the ratio be-tween the gross primary production and the mac-roalgal biomass in the experimental mesocosms.

DOC samples were collected from the septumport of the incubation chambers using acid-washed20-ml syringes filtered through precombusted(450°C for 4 h) GF/F filters. The acid-washed glassvials receiving the samples were encapsulated withacid-washed silicone-Teflon caps. Samples for DOCanalysis were kept frozen until analysis using Pt-catalyzed high temperature combustion on a Shi-madzu TOC-5000A analyzer (Shimadzu Corpora-tion, 3 Kanda-Nishikicho 1-chome, Chiyoda-Ku,Tokyo 101, Japan). Samples were acidified with 2NHCl before injection, and potassium biphthalatewas used to prepare the standard curves. Distilled,UV-radiated water from a Millipore Symplicity ul-trapure water system (Millipore, 36 Antares DriveSuite 280, Nepean, Ontario K2E 7W5, Canada) wasused to prepare the standards and blanks. A seven-point calibration curve between 0 and 400 �M wasused to determine the concentration of DOC in thewater samples from the incubations. The accuracyof the measurements was confirmed to be �2.9�mol DOC using 44–45 �mol DOC and 2 �molDOC ocean water standards provided by Dennis A.Hansell and Wenhao Chen (University of Miami).

The volume of each incubation chamber was de-termined by injecting 5 ml of a 0.25M phosphatesolution at the end of the experiment. The phos-phate solution was allowed to mix for 5 min, and a5-ml sample of enclosure water was collected forspectrophotometric determination (Hansen andKoroleff 1999) of the resulting phosphate concen-tration (final concentration about 200 �M). Thedilution factor was then used to calculate the vol-ume of each chamber, which ranged between 5 and12 l.

The algal material enclosed in the incubationchambers was harvested at the end of the experi-ments, cleansed of detritus, and dried at 95°C toestimate biomass as dry weight. Plant biomass wasconverted from dry weight to units of carbon usingempirically determined conversion factors for eachspecies (N. Marba unpublished).

Whole-System Carbon Budget

The metabolism of each major algal group (brown,red, and green) was determined by incubating themseparately in 20-l closed transparent perplex con-tainers. Each algal group was measured simulta-neously in all eight mesocosms. In each container, asubmersible oxygen sensor (ABB model 9408, con-nected to ABB model 4640-800 transmitters, ABBKent Taylor Limited, Oldends Lane, Stonehouse,

Gloucestershire, GL103TA, UK) was fixed. Smallsubmersible pumps inside the containers producedmild mixing of the contents and a sufficient waterflow near the sensor for accurate oxygen measure-ments. Measurements (of oxygen and temperature)were taken at 30-sec intervals and stored as 15-minaverages. In addition, light intensity in the air wasrecorded. Net production (NP) was determinedfrom the changes in oxygen concentrations be-tween 0 and 24 h. R was determined as the averageof the changes in oxygen concentrations during the1st and 2nd night of the 36-h incubation period.GPP was calculated as the sum of NP and R.

After the incubation, the dry weight of the incu-bated plant material was determined and theweight-specific productions were calculated. Bymultiplying these with the total basin biomass ofeach algal groups, the whole basin metabolism andthe contribution of each algal group were calcu-lated. The estimated system respiration term is aconservative estimate and does not account for thecontribution of macrofauna, which was considerednegligible.

The input of particulate organic carbon was esti-mated from the product of the average POC con-centration in the inflowing waters and the dailywater discharge into the basins. POC output wasestimated from the product of the average POCconcentration in the outflowing waters of each me-socosm and the daily water discharge from the ba-sins. The POC concentration was measured on par-ticles retained after filtering a variable volume ofwater (3 l) sampled within 2 days of the experi-ments to determine the community organic carbonbudget, onto precombusted GF/C filters using aCHN analyzer. The daily POC export was calculatedas both the export of microscopic material and theexport of coarse particulate carbon. The export ofcoarse particulate matter (mainly detached and de-trital algal material) was measured by mountingmesh bags (mesh size, 5 mm) on the outlets of eachmesocosm. The bags were kept at the outlets for24 h, and the material thus collected was rinsed andsorted into brown, red and green algae. The sampleswere dried at 95°C for 24 h and finally analyzed fortissue carbon according to the method describedabove. There was no sediment accumulation in themesocosms, so net retention of organic carbon inthe sedimented material was assumed to be zero.

Whole-system net DOC production in the basinswas calculated from the concentration changes inthe mesocosms between low and high tide, cor-rected for DOC inputs in the inflowing water duringthe tidal cycle. DOC export was then calculated asthe sum of the DOC inputs (that is, DOC inputs in


the inflowing water plus the concentration changeover the residence time of water in the mesocosms).Samples for DOC analyses were collected, stored,and processed as described above.

RESULTS

Metabolism and Net DOC Production of theF. serratus Community

The biomass of the Fucus serratus community at thetime of metabolic and net DOC production ratedetermination varied 20-fold (242–4841 g DWm�2) between the mesocosms, independent of thenutrient concentration (Pearson correlation coeffi-cient, r � 0.25, P � 0.59). The gross production ofthe F. serratus communities averaged (�SE) 2.65 �0.33 g C m�2 d�1 and varied twofold among themesocosms (Table 1), independent of the experi-mental nutrient concentration (r � 0.18, P �0.68) (Figure 1) and the mean biomass of the F.serratus communities (r � �0.09, P � 0.85) in themesocosm. Community respiration varied threefoldbetween mesocosms, averaging 2.06 � 0.25 g Cm�2 d�1, and was also independent of the experi-mental nutrient concentration (r � 0.28, P �0.53) (Figure 1), the gross production (r � 0.60,P � 0.15), and the mean biomass of the F. serratuscommunities (r � 0.72, P � 0.06). The F. serratuscommunities were, in general, autotrophic, with anaverage net production of 0.59 � 0.27 g C m�2 d�1,except for the mesocosm receiving the second-highest nutrient input (dissolved inorganic nitrogenconcentration � 15.25 �mol l�1), which was het-erotrophic (Table 1). The net community produc-tion was independent of the experimental nutrientconcentration (r � �0.03, P � 0.94) (Figure 1).

All of the F. serratus communities were net DOCproducers (Table 1), both in the dark and the light

(Figure 2). The average net DOC release in the lighttended to be somewhat greater, but not signifi-cantly so (r � 0.22, P � 0.63), than in the dark(mean � SE � 0.026 � 0.008 g C m�2 h�1 and0.015 � 0.004 g C m�2 h�1, respectively) (Figure2). Calculations of the net daily DOC release yieldedan average of 0.41 � 0.08 g C m�2 d�1, remarkablyclose to the estimated net production of the F. ser-ratus communities. These data indicated, therefore,that most (average, 69%) of the net production ofthe F. serratus community was released as DOC. Thenet DOC release during the day increased signifi-cantly with increasing experimental nutrient con-centrations (r � 0.88, P � 0.008), whereas releasein the dark was independent of experimental nu-trient inputs (r � �0.08, P � 0.86) (Figure 2).

Whole-System Carbon Budget

The whole-system metabolism in the experimentalecosystems was independent of the nutrient treat-ment (P � 0.8), all experimental ecosystems beingautotrophic (Table 2). The whole-system gross pro-duction (Table 2) was substantially higher, fivefoldon average, than for the F. serratus communityalone (Table 1), whereas the average whole-systemrespiration rate was four times higher than that ofF. serratus (Tables 1 and 2). This difference mayderive from contributions from other communitiespresent in the basin (for example, F. vesiculosus, redand green algae, periphyton).

The total macroalgal biomass in the mesocosms 2years after the initiation of the experimental nutri-ent additions was also independent (r � �0.30,P � 0.51) of the experimental nutrient inputs (Ta-ble 2). In all mesocosms, total biomass showed atendency toward a long-term decline (average,0.18 � 0.06 g C m�2 d�1), a trend that was also

Table 1. Dissolved Inorganic Nitrogen (DIN) Concentration (�mol l�1), Gross Primary Production (GPP),Respiration (R), Net Community Production (NCP), and Net Daily Dissolved Organic Carbon (DOC)Production of the Fucus serratus–dominated Community in the Experimental Mesocosms in August 2000

DIN(�mol L�1)

GPP � SE(g C m�2 d�1)

R � SE(g C m�2 d�1)

NCP � SE(g C m�2 d�1)

DOC daily � SE(g C m�2 d�1)

3.6 2.0 0.4 1.2 0.4 0.8 0.2 0.4 0.14.1 3.3 0.2 2.3 0.2 1.0 0.1 0.4 0.25.0 3.9 0.4 2.6 0.4 1.3 0.1 0.1 0.16.8 1.5 0.2 1.2 0.3 0.3 0.1 0.1 0.1

10.4 2.4 0.5 2.1 0.7 0.3 0.4 0.6 0.315.3 2.1 0.4 2.9 0.3 �0.8 0.3 0.6 0.132.8 3.3 0.4 2.2 0.3 1.1 0.2 0.6 0.1


independent (r � �0.51, P � 0.24) of the nutrienttreatment (Table 2).

The average POC input to the mesocosms duringthe measurement period was estimated at 4.06 �0.51 g C m�2 d�1, whereas the export was slightlyhigher, averaging 5.10 � 0.55 g C m�2 d�1, ofwhich macroscopic and microscopic material ac-counted for 2.94 � 0.50 g C m�2 d�1 and 2.16 �0.15 g C m�2 d�1, respectively. Mesocosm DOC

concentrations averaged 172.3 � 4.8 and 248 � 7.3�mol l�1 at the minimum and maximum waterlevel (“low” and “high tide,” respectively) and wereindependent of nutrient treatments (P � 0.8). Wemeasured the average DOC input to the mesocosmswith the inflowing waters to be 13.32 � 0.18 g Cm�2 d�1 and the DOC output to be 17.12 � 0.81 g

Figure 1. Relationship (mean � SE) between gross pri-mary production (GPP), net community production(NCP), and respiration (R), of the Fucus serratus–domi-nated community and dissolved inorganic nitrogen con-centrations in the experimental mesocosms. Values rep-resent the mean � SE of four to five replicate chambers ineach mesocosm.

Figure 2. Relationship (mean � SE) between net DOCproduction under dark and light incubation, net dailyDOC production of the Fucus serratus–dominated com-munity, and dissolved inorganic nitrogen concentrationsin the mesocosms. The solid line shows the fitted linearregression equation.


C m�2 d�1, thus, the average net DOC productionwas 3.80 � 0.31 g C m�2 d�1 within the mesocosms(P � 0.001), independent of nutrient inputs (P �0.3). The whole-system net DOC production wasalso fivefold higher than for the F. serratus commu-nity alone (Table 1).

DISCUSSION

Our results show that the macroalgal-dominatedexperimental ecosystems in our study are highlyproductive, autotrophic communities. Whole-sys-tem production was extremely high. It was fivetimes greater than the F. serratus community, due,at least in part, to the fact that other brown algalspecies, together with red and green algal commu-nities, were more productive per unit biomass thanthe F. serratus community (M. F. Pedersen unpub-lished). There was, however, no evidence of a sig-nificant ecosystem response to the experimentalnutrient inputs, whether in terms of community orecosystem biomass, metabolism, or net DOC pro-duction. Although green algae showed significantresponses to increased nutrient inputs in terms ofincreased biomass and growth rates (Bokn and oth-ers forthcoming), these responses were negligible atthe ecosystem level due to the low contribution(average, 4.3 � 0.5%) of green algae to the biomassof the experimental communities (N. Marba un-published). Lack of effects of long-term experimen-tal nutrient enrichment on carbon flow and bio-mass in the rocky shore mesocosms is indicative ofmodest or absent nutrient limitation under ambientconditions as well as the high resistance of therocky shore communities investigated. Average nu-trient concentrations were indeed high in the fjordwaters feeding the control mesocosms (Bokn andothers 2002) which, together with the short resi-dence time of the water, may have led to a nutrient

supply that was sufficient to support the very highproduction of the experimental ecosystems. Hence,the observed responses may be buffered relative tothose possible from similar experiments conductedin more oligotrophic waters. These observationsare, however, in line with previous reports of lim-ited effects of nutrient inputs to rocky shore eco-systems (see, for example, Wootton 1991).

The production of the experimental ecosystemwas very high, similar to the range reported forFucus communities elsewhere, which rank amongthe most productive communities in the biosphere(Mann 2000). Although nutrient concentrations inthe ambient waters were very low during the sum-mer, the nitrogen content in the Fucus tissues re-mained high, above 2% of dry weight (M. F. Ped-ersen unpublished), which is believed to be thethreshold below which nutrient limitation occurs(Duarte 1992). Phosphorus contents were, how-ever, low (below the threshold level of 0.2 %)(Duarte 1992) at low phosphate input rates andincreased with increasing nutrient inputs (Boknand others forthcoming), suggesting phosphoruslimitation of macroalgal growth.

Although both the F. serratus communities andthe entire experimental ecosystems were net au-totrophic (average P/R ratio, 1.33 � 0.12 and2.04 � 0.28, respectively), there was no evidence oforganic carbon accumulation in the system, evenconsidering extended (2 years) observational peri-ods. This suggests that carbon was exported at highrates in the form of POC or DOC. The DOC pro-duced by the F. serratus community (average,0.41 � 0.08 g C m�2 d�1) was sufficient to accountfor most (69%, on average) of the net communityproduction (average, 0.59 � 0.27 g C m�2 d�1)(Figure 3). Consequently, very little net productionwas left (after accounting for loss of plant frag-ments) for accumulation in the community as POC,

Table 2. Dissolved Inorganic Nitrogen (DIN) Concentration, Total Macroagal Biomass, Rate of Change inTotal Algal Biomass, Gross Primary Production (GPP), and Community Respiration (R) in the ExperimentalRocky Shore Ecosystems

DIN(�mol l�1)

Biomass(g C m�2)

Net biomass change(g C m�2 d�1)

GPP(g C m�2 d�1)

R(g C m�2 d�1)

3.6 288.7 �0.3 17.8 5.94.1 267.8 �0.2 14.5 5.15.0 546.2 0.0 12.9 12.46.8 368.2 �0.2 9.7 7.0

10.4 309.3 �0.1 12.9 5.515.3 473.2 0.0 17.1 10.132.8 214.9 �0.5 14.2 7.2


whether in plant or animal (micro- or macroscopic)form. Net DOC release by the F. serratus communityrepresented 15% of the plant’s gross production,which is consistent with the percent DOC releasefrom macroalgae as observed in single-organismexperiments (for example, 1%–39 % of the grossproduction) (Khailov and Burlakova 1969; Brilin-sky 1977; Pregnall 1983; Mann 2000).

Export of POC from the mesocosms was not ex-pected to be dominated by algal fragments, becausethe algae are relatively slow growing (average P/Bratio, 0.044 � 0.006 d�1, or a turnover time ofabout 22 days), and a substantial loss would quicklydecimate the populations. The export of coarse ma-terial—largely algal fragments (average, 2.94 �

0.55 g C m�2 d�1)—was, however, a significantsource of organic carbon export. The long-term bio-mass erosion (average, 0.18 � 0.06 g C m�2 d�1)made a minor contribution to the export. Becausethe inputs of fine POC exceeded the outputs, thenet POC export (that is, POC outputs–inputs) ac-counted for only about 1 g C m�2 d�1, or 15% ofthe net ecosystem production (Figure 3). Consistentwith the community-level experiments, the netDOC export was the major source of organic carbonlosses from the ecosystems, comprising about 27%and 58% of the gross and net ecosystem produc-tion, respectively, and 77% and 78% of the grossand net organic carbon export (Figure 3). The con-sideration of DOC export allowed closing of thebudget between organic carbon inputs (31.70 �1.16 g C m�2 d�1) and outputs (29.82 � 1.40 g Cm�2 d�1) from the mesocosms. The net DOC pro-duction was therefore sufficient to balance the car-bon budgets of both the F. serratus community andthat of the experimental ecosystems (Figure 3).

The results presented here provide evidence thathigh carbon export may buffer the response ofrocky shore ecosystems to increased nutrient in-puts. However, these results, derived from a meso-cosm experiment, may not be fully extrapolatableto nature. The scaling of results derived from me-socosm experiments to nature is not trivial, since itdepends on the physical dimensions of the meso-cosm (for example, Petersen and others 1997), aswell as the particular design (for instance, pulsedversus continuous nutrient inputs, and so on). Inparticular, the configuration of our mesocosms mayoverestimate export, because they were designed assemi-flowthrough systems, whereas in tidal-domi-nated environments, some of the exported materialmay return with the returning tidal flow.

Extrapolation of these results to nature there-fore, requires, verification. In particular, the re-sults are expected to vary depending on the dom-inant macroalgae in the community. Thosedominated by perennial algae, such as the onedescribed here, are indeed expected to be resilientand to show little temporal variation in carbonbudgets. In contrast, those dominated by ephem-eral green algae may experience great fluctua-tions, with periods of rapid biomass buildup andcatastrophic decline, and are likely to show verydifferent responses to nutrient inputs than thosereported here (for example, see Hauxwell andothers 1998; Bokn and others forthcoming). Theresponse of macroalgal-dominated communitiesto increased nutrient inputs may therefore bedifferent for rocky shores in the temperate topolar zone dominated by brown perennial mac-

Figure 3. Box models representing the organic carbonbudget of the Fucus serratus–dominated community andthat of the experimental rocky shore ecosystems. GPP,gross primary production; R, community respiration;NCP, net community production; POC, particulate or-ganic carbon; DOC, dissolved organic carbon; � Biomass,net rate of biomass loss. All values in g C m�2 d�1. Valuesare given as mean � SE.


roalgae (for example, fucoids, kelps, and Cysto-seira beds in the Mediterranean) than it is forestuaries and tropical sandy shores, where greenalgae (for example, Ulvales and Caulerpales) aremore likely to dominate (for example, Lobbanand Harrison 1997).

The carbon budget reported here represents theshort-term balance of the community and doesnot necessarily apply to all seasons. However, themesocosms were dominated by perennial mac-roalgae, in terms of both biomass and production,which showed only modest biomass fluctuationsthroughout the year. In addition, the mesocosmproduction remained relatively uniform amongyears (Bokn and others forthcoming). The long-term trends are also incorporated into the budgetthrough the net rate of biomass change, deter-mined over the 27 months of the experimentprior to the budget construction.

In summary, our results provide evidence, bothat the community and experimental ecosystemlevel, of limited effects from long-term nutrientinputs on the carbon flow of experimental rockyshore ecosystems, which were therefore unlikelyto be nutrient-limited. These results lead us tosuggest that the paucity of observational or ex-perimental evidence on the consequences of eu-trophication for rocky shore, macroalgal-domi-nated communities may derive from a paucity ofobservations of eutrophication-related problemsin these ecosystems. Indeed, eutrophication-re-lated problems, such as seagrass loss or water-quality deterioration, have been the main driversof research in this area, and biases in effort allo-cation have been shown to reflect differences inthe incidence of problems (Vidal and others1999). Eutrophication problems are usually de-rived from excess accumulation of micro- andmacroscopic algal biomass (for example, see Du-arte 1995; Valiela and others 1997). Such anaccumulation of biomass was, however, not evi-dent in the experimental rocky shore communi-ties examined here, due to the high net produc-tion and subsequent export of DOC. Our resultssuggest that the export as DOC of a sizeable frac-tion of the production of rocky shore communi-ties, which rank among the most productive inthe biosphere (Valiela 1995; Duarte and Cebrian1996; Mann 2000), is an important regulatoryprocess that also provides a link between theseecosystems and adjacent marine ecosystems.

ACKNOWLEDGMENTS

This research was supported by the EULIT (Effectsof eutrophicated seawater on rocky shore ecosys-

tems studied in large litteral mesocosms) project(contract MAS3-CT97-0153), which is funded bythe MAST III program of the European Commis-sion. C.B. was funded by a scholarship from thegovernment of the Balearic Islands. We thank all ofthe project participants for their collaboration anduseful advice.

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