The Response of ExperimentalRocky Shore Communities to

Nutrient Additions

Tor L. Bokn,1* Carlos M. Duarte,2 Morten F. Pedersen,3 Nuria Marba,2

Frithjof E. Moy,1 Cristina Barron,2 Birger Bjerkeng,1 Jens Borum,4

Hartvig Christie,5 Silke Engelbert,7 Frank L. Fotel,3 Espen E. Hoell,6

Rolf Karez,7 Kees Kersting,8 Patrik Kraufvelin,9 Cecilia Lindblad,Marianne Olsen,6 Knut Arvid Sanderud,6 Ulrich Sommer,7 and

Kai Sørensen10

1Norwegian Institute for Water Research (NIVA), P.O. Box 173, Kjelsaas, N-0411 Oslo, Norway; 2Grupo de OceanografiaInterdisciplinar, Instituto Mediterraneo de Estudios Avanzados (CSIC-UIB), C/Miquel Marques 21, 07190 Esporles, Spain;3Department of Life Sciences and Chemistry, Roskilde University, P.O. Box 260, DK-4000 Roskilde, Denmark; 4Freshwater

Biological Laboratory, University of Copenhagen, Helsingørsgade 51, DK-3400 Hillerød, Denmark; 5Norwegian Institute for NatureResearch (NINA), P.O. Box 736 Sentrum, N-0105 Oslo, Norway; 6Norsk Hydro ASA, Porsgrunn Research Center, P.O. Box 2560,

N-3901 Porsgrunn, Norway; 7Institut fur Meereskunde, Abteilung Meeresbotanik, Universitat Kiel, Dusternbrooker Weg 20 D-24105, Kiel, Germany; 8Marine and Coastal Zone Research Team, ALTERRA, P.O. Box 167, 1790 AD Den Burg (Texel), The

Netherlands; 9Environmental and Marine Biology, Abo Akademi University, Akademigatan 1, FIN-20500 Turku/Abo, Finland;10Department of Botany, Stockholm University, Stockholm, Sweden

ABSTRACTThe aim of this study was to determine whether theexperimental nutrient enrichment of littoral rockyshore communities would be followed by a pre-dicted accumulation of fast-growing opportunisticalgae and a subsequent loss of perennial benthicvegetation. Inorganic nitrogen (N) and potassium(P) was added to eight concrete mesocosms inhab-ited by established littoral communities dominatedby fucoids. The response to nutrient enrichmentwas followed for almost 2 1/2 years. Fast-growingopportunistic algae (periphyton and ephemeralgreen algae) grew significantly faster in response tonutrient enrichment, but the growth of red fila-mentous algae and large perennial brown algae wasunaffected. However, these changes were not fol-lowed by comparable changes in the biomass andcomposition of the macroalgae. The biomass of op-portunistic algae was stimulated only marginally bythe nutrient enrichment, and perennial brown al-

gae (fucoids) remained dominant in the mesocosmregardless of nutrient treatment level. Establishedrocky shore communities thus seem able to resistthe effects of heavy nutrient loading. We found thatthe combined effects of the heavy competition forspace and light imposed by canopy-forming algae,preferential grazing on opportunistic algae by her-bivores, and physical disturbance, succeeded by amarked export of detached opportunistic algae, pre-vented the fast-growing algae from becoming dom-inant. However, recruitment studies showed thatthe opportunistic algae would become dominantwhen free space was available under conditions ofhigh nutrient loading and low grazing pressure.These results show that established communities ofperennial algae and associated fauna in rocky shoreenvironments can prevent or delay the accumula-tion of bloom-forming opportunistic algae and thatthe replacement of long-lived macroalgae by oppor-tunistic species at high nutrient loading may be aslow process. Nutrient enrichment may not, in it-self, be enough to stimulate structural changes inrocky shore communities.

Received 23 January 2002; accepted 22 October 2002; published online 9September 2003.*Corresponding author; e-mail: tor.bokn@niva.no

Ecosystems (2003) 6: 577–594DOI: 10.1007/s10021-002-0108-6 ECOSYSTEMS

© 2003 Springer-Verlag

577

Key words: mesocosm; hard-bottom organisms;intertidal communities; nutrient enrichment;coastal eutrophication; rocky shore communities;algae; benthic vegetation.

INTRODUCTION

Coastal ecosystems rank among the most produc-tive biomes on Earth (Mann 1982), but the inten-sified use of fertilizers over the last century has leadto the eutrophication and destruction of ecosystemstructure and function in many coastal areas (Nixon1995; Richardson and Jørgensen 1996). Because ofthe serious ecological and socioeconomic conse-quences of coastal eutrophication, a wealth of stud-ies on the effects of nutrient enrichment have beeninitiated over the last 3 decades (Nixon 1995; Vidaland others 1999). Most of these studies have fo-cused on the response of phytoplankton andephemeral macroalgae in the pelagic (see for exam-ple Ryther and Dunstan 1971; Graneli and others1986; Hecky and Kilham 1988; Nixon 1992; Rich-ardson and Heilmann 1995) or shallow estuarineenvironment (for example see reviews by Fletcher1996; Short and Wyllie-Echeverria 1996; Raffaelliand others 1998).

Nutrient enrichment stimulates phytoplanktonproductivity and the increase of biomass in pelagicsystems (Hecky and Kilham 1988), leading to in-creased sedimentation of organic matter, oxygendeficiency in deeper water, and lower ecosystemdiversity (Richardson and Jørgensen 1996). In shal-low estuarine areas and lagoons, eutrophicationstimulates the bloom of phytoplankton, epiphytes,and ephemeral macroalgae and is followed by theloss of long-lived benthic macroalgae and seagrasses(Duarte 1995; Schramm 1999). Total system pro-ductivity in estuaries is rarely affected by nutrientenrichment (Borum and Sand-Jensen 1996), butthe structural changes engendered by eutrophica-tion increase the turnover of nutrients and oxygen.This may lead to more frequent events of oxygendepletion and the subsequent loss of fauna (Sand-Jensen and Borum 1991; D’Avanzo and Kremer1994).

Because the effects of eutrophication seem lesspronounced in exposed rocky shore ecosystems(see for example, Niell and others 1996), they havereceived less attention (Vidal and others 1999).However, a few observational studies have detectedchanges in species composition and depth distribu-tion among rocky shore macroalgae after increasednutrient loading (for example, Littler and Murray1975; Kautsky and others 1986; Rueness andFredriksen 1991; Bokn and others 1992; Munda

1996). Rocky shore systems may be less sensitive tonutrient enrichment because they differ from shal-low, sheltered estuaries and lagoons with respect towater exchange, physical exposure (waves), andcommunity structure. In these systems, rapid waterexchange may dilute nutrient concentrations closeto point sources considerably and facilitate the ex-port of pelagic and detached components (for ex-ample, phytoplankton and free-floating macroal-gae). Furthermore, intermediate to high waveexposure may “clean” the substrate for ephemeralalgae (Sousa 1979, 1980), which are more fragilethan the fucoids and kelps that normally dominatethese communities (Littler and Littler 1980). Fi-nally, rocky shore systems are densely inhabited bylarge grazers such as snails, limpets, sea urchins,and fish, which may cause significant grazing lossesto macroalgae (Lubchenco and Gaines 1981; Un-derwood and Jernakoff 1984).

Most experimental evidence of the effects of eu-trophication on coastal ecosystems comes fromsmall-scale studies. Although small-scale experi-ments are adequate means of assessing physiologi-cal responses to nutrient enrichment at the organ-ism level or examining species interactions (that is,competition, grazing), they are too limited to ad-dress the complicated structure of natural commu-nities or the feedback processes that occur in na-ture. Thus, although they are useful for theinvestigation of relationships underlying processesat higher levels, the results may be oversimplifiedand not fully scaled to these higher levels. Large-scale experimental manipulation that includes en-tire communities or whole ecosystems (that is, me-socosms) is therefore preferable, but for logistic andeconomic reasons, it is seldom possible on rockyshore communities.

The use of mesocosms has improved our under-standing of the eutrophication processes in pelagic(for example, see Baretta-Bekker and others 1998;Hein and Riemann 1995; Duarte and others 2000;Olsen and others 2001) and soft-bottom ecosystems(for example see Oviatt and others 1993; Brinkmanand others 1995; Taylor and others 1995). How-ever, mesocosms have not yet been used to studyeutrophication effects on rocky shore systems,probably because such systems are difficult to re-produce under controlled conditions. The keystonebiological components of rocky shore ecosystemsare mainly long-lived and require years to establishbefore experiments can be initiated. The energeticenvironment of rocky shore ecosystems, which in-cludes tides and wave action, is also difficult toimplement in mesocosms (Bakke 1990), rendering

578 T. L. Bokn and others

the design of rocky shore mesocosm experimentscumbersome and resource-demanding.

This paper provides a synthesis of the results ob-tained during a 3-year enrichment experiment thatattempted to provide a more robust basis for ourunderstanding of the responses of rocky shore com-munities to increased nutrient loading. Theproject’s objective was to assess the overall responseof littoral rocky shore communities to elevated nu-trient loading and to identify and quantify the pro-cess driving these changes. We expected that en-hanced nutrient loading would (a) stimulate thegrowth and accumulation of fast-growing algae(that is, periphyton and ephemeral macroalgae) atthe expense of slow-growing perennial algae, (b)stimulate the abundance of secondary producersthrough increased availability of high-quality food,and, (c) increase the export of organic matter fromthe system due to the increased dominance of del-icate algae. The experiment was also designed toassess whether the expected structural changeswould be followed by changes in overall primaryproduction.

METHODS

Site Operation and Experimental Setup

The experiment was conducted in eight land-basedmesocosms (Figure 1) designed to support hard-bottom littoral communities at the Marine ResearchStation, Solbergstrand (Oslofjord, Norway). Eachmesocosm contained from 6 to 12 m3 of seawater(low and high tide, respectively) with a tidal ampli-tude of 0.36 m, similar to the mean of the fjord

outside. Each mesocosm was fed with fjord water(pumped from 1-m depth) at a rate of 5 m3 h�1,giving an average water residence time of about 2 h.Waves were generated continuously by a wave ma-chine (17 strokes per min). A technical descriptionof the mesocosm facility is presented in Bokn andothers (2001).

The experimental littoral communities were es-tablished by introducing small boulders with asso-ciated macroalgae and fauna from the Oslofjordinto the mesocosms 2 years prior to the start of theexperiment. The import of algal spores and animallarvae with the inflowing seawater ensured thecontinuous development of the communities dur-ing the preproject period and resulted in a flora andfauna resembling that of the littoral zone in theOslofjord.

Nutrient enrichment was initiated in May 1998and lasted for 27 months. Inorganic nitrogen (N)and phosphorus (P) was added continuously to sixof eight basins from stock solutions of H3PO4 andNH4NO3 at target concentrations of 1, 2, 4, 8, 16,and 32 �M dissolved inorganic N (DIN) and 0.06,0.13, 0.25, 0.5, 1.0, and 2.0 �M dissolved inorganicP (DIP) above the background concentrations of theinflowing water. The dissolved nutrients werepumped into each basin from specifically madestock solutions using a dosing pump (Watson Mar-low 505 S) with a feeding rate of 1 ml min�1 (seeBokn and others 2001 for details on the nutrientmanipulation). Annual N and P loading (that is,ambient plus added nutrients) ranged from 28 to109 moles N m�2 and from 1 to 6 moles P m�2,respectively (Table 1). Nutrient concentrations in

Figure 1. Diagram ofone of the eight meso-cosms with intertidalorganisms attached tosmall boulders and stepsmimicking intertidal lev-els. Water input isthrough a pipe at thenorth/east (uppermost)corner; the outlet is inthe southeast (leftmost)corner through the tidalregulator tube.

Response of Rocky Shore Communities to Nutrients 579

the inflowing water and in each basin were mea-sured on a weekly basis in pooled samples (fivesamples per week). The samples were preservedand analyzed according to standard methods (seeBokn and others 2001 for details).

Measurements

Community structure (that is, abundance, biomass,and species composition), physiological properties(nutrient content and growth), and communityprocesses (that is, production and grazing rates, re-cruitment and early development, export and sys-tem metabolism) were surveyed during seven in-tensive field campaigns (spring, summer, andautumn 1998 and 1999 and summer 2000), eachlasting for 2–3 weeks.

Algal and fauna biomass and composition. Mac-roalgal cover was measured in 16 quadrates (42 �42 cm, each divided into 25 subquadrates) forminga fixed grid system in each basin. Cover estimateswere transformed to units of biomass using species-specific biomass per unit of cover ratios, obtainedthrough destructive subsampling outside the per-manent sampling area. Subsamples of all macroal-gal species were collected from each basin for thedetermination of carbon (C), N, and P content.Samples were cleaned, dried (80°C for 48 h), andanalyzed for total C and N using a Carlo-Erba NA-1500 elemental analyzer. Total P content was de-termined by means of a modified Kjeldahl proce-dure using standard colorimetric methods(Grasshoff and others 1983) after oxidation withH2SO4.

Total periphyton biomass was quantified only inAugust 2000. Four samples of periphyton were col-lected from each of the dominant surface types(that is, dominant species of perennial macroalgae,

boulders, and concrete surfaces) in all mesocosmsand analyzed for chlorophyll content (Lorenzen1967). Total periphyton biomass per mesocosm wascalculated by multiplying substrate-specific per-iphyton biomass (per unit of area) by the totalsurface area of each substrate type. Chlorophyllbiomass was finally converted to dry weight (DW)biomass assuming a C/Chl ratio of 75 and a C con-tent of 50% of DW.

Recruitment and early development of macroal-gal communities were studied from settling andsubsequent development of macroalgae on “clean”substrates (that is, 10 � 10 cm granite tiles). Thetiles were mounted in four of the eight basins(treatment levels, �0, �2, �8, and �32 �M N) atthe start of the experiment (April 1998) and placedon permanent steel racks 10 cm below the watersurface at low tide. The design of these racks en-sured that the tiles were inaccessible to benthicgrazers, such as gastropods. Three tiles were har-vested from each basin every 2nd month betweenApril and October during the entire experiment,and cover, biomass, and species composition werequantified on each tile.

The abundance of large mobile and sessile ani-mals in the mesocosms was determined by countingall individuals within the quadrates used to assessmacroalgal cover. The abundance of small mobileanimals (macro- and meiofauna) was quantifiedusing artificial substrates (“traps,” n � 8 in eachbasin per sampling event) located at differentdepths in the mesocosms and by direct samplingfrom dominant species of macroalgae (four species,n � 4 in each basin). The total abundance of eachfauna group was estimated for each mesocosm bymultiplying the substrate-specific abundances bythe total proportion of different substrates (includ-

Table 1. Nitrogen (N) and Potassium (P) Loading Rates at Different Treatment Levels

Treatment P loading N loading

�mole Nand Pl�1

mol P basin�1

d�1mol Pm�1 y�1

mol Nbasin�1 d�1

mol N m�2molN�2y�1

Basins 1 and 8 �0/�0.00 0.039 0.82 (0.74) 1.32 27.7 (0.65)Basin 4 �1/�0.063 0.047 0.98 (0.62) 1.44 30.3 (0.60)Basin 5 �2/�0.13 0.054 1.14 (0.53) 1.56 32.8 (0.55)Basin 6 �4/�0.25 0.069 1.46 (0.42) 1.80 37.8 (0.48)Basin 3 �8/�0.50 0.099 2.09 (0.29) 2.28 47.9 (0.38)Basin 7 �16/�1.00 0.159 3.35 (0.18) 3.24 68.1 (0.26)Basin 2 �32/�2.00 0.279 5.88 (0.10) 5.16 108.6 (0.17)

Values are mean values (averaged over the experimental period May 1998–August 2000).Numbers in brackets are Coefficients of variation (CVs), describing the temporal variation. Nutrient loading rates were estimated from the nutrient concentrations of the inletwater, the amount of added nutrients, and the water flow rate into each basin (5 m3 h�1).

580 T. L. Bokn and others

ing algal groups) in each mesocosm. Finally, totalfauna biomass was estimated from standardizedweight analyses of each species.

Algal growth and primary production. Net growthrates of four species of macroalgae (Ulva lactuca,Ceramium rubrum, Fucus vesiculosus, and F. serratus),each of which was a quantitatively importantand/or typical representative of a specific type ofalgae, were measured from the increase in biomassof subsamples placed in transparent cages for 10–12days. The cages were made of Perspex (20 cm long,10 cm in diameter) and closed at both ends withmesh (mesh size, 1.0 mm) to exclude mesoherbi-vores and prevent the loss of algal material. Thecages were placed approximately 30 cm below thewater surface at low tide. Growth rates (�) wereestimated according to the following equation:

� �ln BT � ln B0

t(1)

where BT and B0 are the final and initial bio-mass and t is the incubation time. Six replicatemeasurements of growth (for each of the ex-amined species) were carried out in each me-socosm during each campaign.

Growth of the periphyton community was mea-sured from the accumulation of periphyton biomasson small ceramic tiles exposed for 15–20 days ineach basin. Four “clean” tiles (each 5 � 5 cm) werefixed to a vertical holder that was accessible toswimming grazers but not to benthic grazers, suchas Littorina spp. The amount of chlorophyll accu-mulated on the tiles and the C, N, and P content ofthe periphyton communities were determined fol-lowing the methods of Lorenzen (1967) and Hill-ebrand and Sommer (1997). Growth was estimatedfrom changes in biomass over time according to Eq.(1).

Each mesocosm was permanently equipped witha submersible oxygen and temperature sensor(ABB model 9408), and a ninth sensor was placedin the inflow pipe from the Oslofjord. Measure-ments of oxygen and temperature from each meso-cosm were taken at 30-s intervals and stored as15-min averages in a datalogger; light intensity(PAR) in the air was recorded (LiCor model Li-190SA) with the same frequency. Total mesocosmmetabolism—that is, gross primary production(GPP) and total mesocosm oxygen consumption,including algae, animals, and microorganisms—wascalculated from the dial changes in oxygen concen-tration (for technical details, see Bokn and others2001).

Additionally, the oxygen metabolism of each ofthe major algal groups (Ulva lactuca, Ceramium

rubrum, and Fucus vesiculosus) was measured in eachmesocosm and campaign. Subsamples of algae wereincubated in 20-L submersed closed transparentPerspex containers, each equipped with an oxygensensor. The measurements for each algal groupwere performed simultaneously in all eight meso-cosms for 36 h. Measurements of oxygen and tem-perature from each container were taken at 30-sintervals and stored as 15-min averages in a data-logger. PAR in the air was recorded with the samefrequency.

Net primary production (NPP) was calculatedfrom changes in oxygen concentration between 0and 24 h, and respiration (R) was estimated fromthe average of changes in oxygen concentrationduring the 1st and 2nd night of the 36-h incubationperiod. GPP was calculated as the sum of NPP andR. Finally, the dry weight of the incubated algaewas determined, and biomass-specific productionrates were calculated. Total metabolism (per basin)and the contribution from each algal group werecalculated by multiplying the biomass-specific ratesby the total biomass of each algal group (per basin).

Grazing losses. Potential consumption rates ofthe most important herbivores were determinedfrom “enclosure” measurements placed within themesocosms. Subsamples (1–5 g DW) of Ulva lactuca,Ceramium rubrum, Fucus vesiculosus, and F. serratusand small ceramic chips covered by periphytonwere incubated for 10–12 days together with fourto eight individuals of Littorina littorea, Idotea granu-losa, or Gammarus locusta in transparent Perspexcages (20 cm long, 10 cm in diameter) closed atboth ends with mesh (mesh size, 1.0 mm). Sixreplicate incubations were carried out for each an-imal species in each mesocosm. Species-specificconsumption rates were estimated from changes inalgal biomass during the incubation after correctingfor biomass changes due to growth. Consumptionrates were expressed in units of mg alga consumedg�1 animal d�1. The consumption rates thus ob-tained were multiplied by fauna abundance (perbasin) to estimate total potential consumption ofeach algal type in the mesocosms.

Export of organic matter from the mesocosms. Exportof coarse material (CPOC) (greater than 1 mm)from the mesocosms was quantified on 36 occa-sions during the experiment. The outlet water fromeach mesocosm was led through a 1-mm mesh bagfor 24 h. The bag sample was sorted into main faunaand algal groups (that is, green, red, and brownalgae), dried, weighed, and finally analyzed for Ccontent using a Carlo-Erba NA-1500 elemental an-alyzer. The import and export of fine particulate C(FPOC) (smaller than 1 mm) was determined from

Response of Rocky Shore Communities to Nutrients 581

duplicate water samples (5–10 L) taken from the in-and outflowing water of each mesocosm every 3rdday during each campaign. Each water sample wasfiltered through a preburned Whatman GF/C filter.The filters were dried at 80°C for 48 h, and the Ccontent was subsequently determined using aCarlo-Erba NA-1500 elemental analyzer. The con-centration of dissolved organic carbon (DOC) in thein- and outflowing water of each mesocosm wasmeasured on a weekly basis in pooled water sam-ples (five samples per week) taken from with in theinlet and near the outlet of each mesocosm. Thesesamples were collected 1 week prior to and 1 weekafter each campaign (that is, five pooled samplesper campaign). The water samples were filteredthrough a Whatman GF/C filter, and the concen-tration of DOC was analyzed on the filtrate using aShimadzu TOC-5000 total organic carbon analyzer.Finally, the concentrations of FPOC and DOC weremultiplied by the water flow rates to obtain esti-mates of import and export.

Statistical Analysis

Each experimental unit (that is, the mesocosms)was unreplicated (except for the control treatmentwhere n � 2). The possible effect of nutrient loadingon response parameters (for example, biomass,growth rates, grazing rates, export) could thereforenot be examined by the use of comparative statisticssuch as analysis of variance (ANOVA) (Hurlbert1984). The relationships between the various re-sponse parameters and the nutrient treatment lev-els were instead analyzed by Pearson’s correlationanalysis (Zar 1999). Data were log-transformed asneeded to obtain linearity between the dependentand independent variables.

RESULTS

Nutrient Concentrations

The background concentrations of DIN (NH4� �

NO3�) ranged from 1 �M in midsummer to about

30 �M during winter, and nutrient enrichmentcaused a significant increase in DIN concentrations(Figure 2a). The background concentrations of DIPwere low, ranging from 0.02 �M in summer toabout 0.8 �M during winter (Figure 2b). Nutrientenrichment caused a significant increase in DIPconcentrations. The molar N:P ratios in the inflow-ing water averaged 40.8 � 25.7 (�SD), but theyvaried considerably over the season. The N:P ratioswere close to Redfield’s ratio (Redfield and others1963) in winter, but they increased to 160 in sum-

mer, suggesting strong P limitation during the maingrowing season.

Algal and Fauna Biomass and Composition

Total macroalgal biomass averaged 876 � 332(�SD) g DW m�2 across time (May 1998–August2000) and mesocosms (Table 2). Total macroalgalbiomass varied considerably over the experimentalperiod (Figure 3), but there was no systematic trendin biomass change with nutrient treatment (R �0.005, P � 0.975). The macroalgal assemblageswere dominated by perennial brown algae (partic-ularly Fucus serratus and F. vesiculosus), but the bio-mass of these algae did not vary systematically withnutrient treatment (R � 0.036, P � 0.819). The redalgae were entirely dominated by filamentous spe-cies belonging to the genera Polysiphonia, Ceramium,and Rhodomela. Red algal biomass was very high inspring and summer 1998, but it declined markedlyover the course of the experiment. Variations in redalgal biomass were never correlated to nutrienttreatment level (R � �0.008, P � 0.961). Ephem-eral green algae (mainly Enteromorpha spp. and Ulvalactuca) contributed little to total algal biomass (Ta-ble 2), but their biomass increased significantly withincreasing nutrient loading (R � 0.331, P � 0.032),resulting in twofold higher biomass at higher nutri-ent treatment levels.

This response was even stronger for summer dataonly (R � 0.413, P � 0.061). Total periphytonbiomass (data not shown) ranged from 0.8 to 2.4 gDW m�2 (mean, 1.5) and was positively correlatedwith nutrient treatment level (R � 0.736, P �0.038). Yet the periphyton biomass remained verylow (less than 0.2% of total algal biomass), and thestimulation of periphyton and green algal biomasstherefore had little effect on the overall biomass andcomposition of the algal assemblages.

The weak response in algal biomass and compo-sition led to an apparent stability in macroalgalspecies richness and diversity. The number of mac-roalgal species varied from 16 to 26 across time andtreatment, but the variation was not correlated withnutrient treatment levels.

The recruitment and subsequent developmentof macroalgae on clean granite tiles was luxuri-ant. The total algal biomass on these tiles wassimilar across nutrient treatments during the 1styear of the experiment, but the biomass becameconsiderably larger in the control basin duringthe 2nd and 3rd years of the experiment (around3000 versus less than 1000 g DW m�2). The mac-roalgal assemblages that developed on the tiles atlow nutrient levels became dominated by peren-nial brown algae (Fucus spp.), whereas ephemeral

582 T. L. Bokn and others

green algae were totally dominant at the highestnutrient treatment level (Figure 4). Species rich-ness and diversity tended to increase over time atlow nutrient levels, whereas no change in diver-sity was observed at higher nutrient treatmentlevels (data not shown).

The mesocosms hosted at least 80 taxa of macro-fauna, which was dominated by crustaceans (33taxa) and molluscs (22 taxa) (Kraufvelin and oth-ers, forthcoming). Total macrofauna biomass aver-aged 209 � 81 g DW m�2 across mesocosms andtime and was dominated by mesograzers and filterfeeders. The abundance and biomass of the me-

sograzers experienced considerable seasonal varia-tion, with the highest values observed in summer(Figure 5). Nutrient enrichment had no effect onthe overall abundance and biomass of the fauna (R� 0.090, P � 0.573), but a few species (for example,Littorina littorea) became more abundant at highnutrient loading (Figure 6). Small crustaceans (iso-pods and amphipods) also tended to be more abun-dant (although not significantly so) at the highestnutrient levels (Kraufvelin and others forthcom-ing). Total meiofauna biomass was insignificantrelative to that of the macrofauna, and there wereno systematic variations in abundance, biomass,

Figure 2. The concentra-tions of A dissolved inor-ganic nitrogen (solid line,NH4

�; dashed line, NO3-)

and B phosphorus in theincoming water from theOslofjord and in the waterfrom each mesocosm overthe course of the experi-ment (May 1998–August2000).

Response of Rocky Shore Communities to Nutrients 583

or species composition with increased nutrientloading.

Algal Growth and Primary Production

Mean algal growth rates differed almost 10-foldamong the various types of algae; they were lowestamong the perennial brown algae and highest forperiphyton (Table 3). The growth rates of periphy-ton and Ulva lactuca responded significantly to nu-trient enrichment (Table 4); the response wasstrongest for periphyton, which was stimulated inspring, summer, and autumn, whereas Ulva lactucawas stimulated only during summer. Nutrient en-

richment did not significantly affect the growth offilamentous red algae and the two perennial brownalgae (Fucus vesiculosus and F. serratus).

Estimates of GPP and algal R based on oxygenmetabolism reached 2350 and 1000 g C m�2 y�1,respectively, resulting in an annual net primaryproduction of 1350 g C m�2. This is roughly similarto the estimate of 1300 g C m�2 obtained by com-bining algal biomass and growth data. NPP did notvary systematically with nutrient treatment level(Figure 7). Perennial brown algae, which made up86% of the total algal biomass, were responsible for67% of the total production, whereas periphyton

Figure 2. Continued.

584 T. L. Bokn and others

and ephemeral macroalgae (that is, foliose and fil-amentous algae) contributed somewhat less (al-though substantially) to total net production (3%,18%, and 11%, respectively). The contribution ofperennial brown algae to total primary productionwas negatively correlated to treatment level (R ��0.725, P � 0.042), whereas the contribution ofperiphyton to total production increased with nu-trient treatment level (R � 0.804, P � 0.016). Thecontribution of green and red algae to total produc-tion did not vary systematically with treatmentlevel.

Nutritional Quality and Grazing

The nutritional quality of the algae increased withnutrient enrichment as mean C:P and N:P ratiosdeclined significantly with increasing nutrient load-ing (R � 0.80, P � 0.01 and R � 0.90, P � 0.01,respectively) (Figure 8). Changes in the nutritionalquality of the algae were reflected in the grazingpatterns when compared across algal type and nu-trient treatment (Figure 9). Potential annual graz-ing losses (that is, as extrapolated from enclosureexperiments to the entire system) averaged 682 g Cm�2 but differed markedly among algal groups.Annual grazing losses corresponded to 317% of theperiphyton production, 138% of the green algalproduction, 36% of the red filamentous algal pro-duction, and 25%–30% of the perennial brownalgal production. In all, 54% of the primary pro-duction was removed by herbivores. Relative toalgal productivity, the potential grazing losses in-creased with nutrient loading (R � 0.673, P � 0.068for ephemeral green algae, R � 0.844, P � 0.008 for

filamentous red algae, and, R � 0.821, P � 0.012 forperennial brown algae), showing that the propor-tion of macroalgal production consumed increasedwith nutrient enrichment. By contrast, relativegrazing of periphyton tended to decrease with in-creasing nutrient treatment level (R � –0.630, P �0.094), thus reflecting the fact that periphyton wasable to “escape” nutrient-enhanced grazing via amarked stimulation of growth.

Export and Total Ecosystem Carbon (C)Balance

The average export of macroscopic algal fragmentsfrom the mesocosms reached 210 g C m�2 y�1,corresponding to about 16% of the total net pri-mary production (Table 5). The export of algae didnot vary systematically with nutrient treatmentlevel (R � 0.304, P � 0.398), but the export lossdiffered considerably among the various types ofalgae (56%, 31%, and 5% of the production forgreen, red, and perennial brown algae, respective-ly). The annual export of fauna consisted mainly ofsmall crustaceans and averaged 33 g C m�2,whereas the net export of FPOC and DOC averaged330 g C m�2 y�1. None of these exports variedsystematically with nutrient treatment. Total sys-tem R averaged 1280 g C m�2 y�1 across meso-cosms and was not correlated to nutrient treat-ment.

Total annual NPP averaged 2350 g C m�2,whereas grazing and export of macroscopic algalfragments totaled 890 g C m�2 (Table 5). The re-maining 460 g C m�2 must either have accumu-lated in the basins as detritus, or been lost through

Table 2. Overall Mean Biomass of Brown, Red, and Green Macroalgae Plus Periphytic Microalgae in theMesocosmsa

Treatment Level(�mol N, P N

�1)AllMacroalgae

BrownMacroalgae

RedMacroalgae

GreenMacroalgae

PeriphyticMicroalgae

Mean biomass (g DW m�2) 876 � 332 742 � 271 82 � 117 40 � 23 2 � 1�0/�0.00 1 1 1 1 1�1/�0.063 1.01 � 0.31 0.94 � 0.37 1.02 � 0.61 1.71 � 1.22 0.96�2/�0.13 1.18 � 0.51 1.19 � 0.56 1.01 � 0.63 1.22 � 0.85 0.76�4/�0.25 0.98 � 0.31 0.98 � 0.34 0.62 � 0.37 2.04 � 0.90 0.79�8/�0.50 1.03 � 0.33 1.01 � 0.40 1.06 � 0.45 2.08 � 1.51 1.58�16/�1.00 1.34 � 0.52 1.16 � 0.50 1.01 � 0.50 1.94 � 0.79 1.86�32/�2.00 0.90 � 0.31 0.88 � 0.37 1.06 � 0.58 1.54 � 0.45 1.75Contribution to total biomass (%) 86.0 � 10.9 7.9 � 8.7 5.4 � 3.6 0.2

N, nitrogen; P, potassium; DW, dry weightThe relative response in biomass to nutrient enrichment is also shown for each treatment level (mean values � SD, n � 6). Total biomass of periphytic microalgae was onlyquantified on one occasic August 2000).aAveraged over the experimental period from June 1998 to August 2000

Response of Rocky Shore Communities to Nutrients 585

decomposition, or been exported as FPOC and DOC(330 g C m�2).

DISCUSSION

Results from small-scale enrichment experimentsshow that eutrophication favors fast-growing algaesuch as phytoplankton, periphyton, and ephemeralmacroalgae (Pedersen 1995; Pedersen and Borum1996) because such algae require high nutrient in-puts for rapid growth (for example, see Fujita 1985;Pedersen and Borum 1997). Observational evi-dence confirms that eutrophication of shallow es-tuaries and coastal areas often leads to the bloom ofphytoplankton and other nuisance algae (see, forexample, Raffaelli and others 1998), followed by

increased competition for light and subsequent lossof benthic macrophytes (see reviews by Duarte1995; Valiela and others 1997; Schramm and Nien-huis 1996). However, the strength of this responsevaries considerably among systems and betweenyears due to significant differences in biotic andabiotic conditions (Schramm 1999).

The objective of our experiment was to confirmthe predicted coupling between nutrient enrich-ment and structural changes among primary pro-ducers under controlled conditions. However,heavy nutrient loading did not significantly stimu-late the bloom of opportunistic algae in our exper-iment. The biomass of both periphyton and ephem-eral macroalgae remained low at all treatmentlevels. The mesocosms were completely dominated

Figure 3. Macroalgal biomass and its distribution intodifferent algal groups and nutrient treatment levelsthrough time. (A) Brown algae (mainly fucoids). (B)Red algae (mainly filamentous species). (C) Green algae(mainly Enteromorpha spp. and Ulva lactuca).

Figure 4. The development of macroalgal cover and itspartitioning among main algal groups on “clean” gran-ite tiles exposed to four different nutrient levels sincethe initiation of the experiment in May 1998. (A)Brown algae (mainly fucoids). (B) Red algae (mainlyfilamentous species). (C) Green algae (mainly Enthero-morpha spp. and Ulva lactuca).

586 T. L. Bokn and others

by perennial brown algae (fucoids) before nutrientenrichment was initiated and remained so through-out the entire course of the experiment. Substantialnutrient enrichment had a limited impact on totalalgal biomass, community structure, and total pri-mary production, suggesting that littoral communi-ties in moderately exposed rocky shore environ-ments are resistant to the stress imposed byeutrophication. The result is surprising because itcontradicts the current dogma of eutrophication,which predicts a relatively simple and direct linkagebetween increasing nutrient loading, algal blooms,and the loss of long-lived, benthic vegetation. Themechanisms that prevented the excessive bloomingof ephemeral algae and the subsequent loss of pe-rennial benthic macroalgae, including possiblefeedback processes that may buffer the effects ofeutrophication, must therefore be identified to

reach a more comprehensive understanding of thecoupling between nutrient enrichment and com-munity responses.

Possible Experimental Artifacts

Mesocosms represent a simplification of naturalsystems; thus, the extent to which they can mimicnatural systems, with all their complex interactions,is limited. The absence of a robust response to nu-trient enrichment could therefore have been causedby inherent problems with the experimental setup.

Under natural conditions, phytoplankton bio-mass is stimulated by nutrient enrichment (Heckyand Kilham 1988). The shading effect exerted byphytoplankton adds to the shading imposed by pe-riphyton and ephemeral algae and thus contributesto the loss of long-lived benthic macrophytes

Figure 5. Macrofauna biomass and its distribution intomain feeding types (grazers and filter feeders) at differ-ent nutrient treatment levels and through time. (A)Mesograzers. (B) Filter feeders. (C) Total fauna bio-mass. Filter feeders were not quantified in April 1998.

Figure 6. The abundance of main herbivores at differentnutrient treatment levels and through time. (A) Isopods.(B) Amphipods. (C) Littorina spp.

Response of Rocky Shore Communities to Nutrients 587

(Sand-Jensen and Borum 1991; Duarte 1995). Therelative importance of shading by phytoplankton ishighly variable and depends on water depth andwater retention time (Sand-Jensen and Borum1991; Valiela and others 1997). Therefore, in thisexperiments the negative effects of increasing phy-toplankton biomass were minimized by the lowwater retention time, causing high export of plank-ton and preventing a significant accumulation ofbiomass in the water column. Total shading of thebenthic vegetation was therefore less than would beexpected under natural conditions, which mayhave ameliorated and/or delayed the loss of slow-growing perennial macroalgae. However, the ex-clusion of phytoplankton effects cannot explainwhy other opportunistic algae did not prosper inthe mesocosms after nutrient enrichment.

The growth of opportunistic algae must be nutri-ent-limited under ambient conditions before a re-sponse to nutrient enrichment can be expected.High background concentrations of N and P couldtherefore have prevented a marked response of theephemeral algae to enrichment. N is often consid-ered the most limiting nutrient in northern temper-ate coastal waters; and although average back-ground concentrations of DIN were relatively high,they were low enough (less than 1 �M) to rendermost ephemeral algae N-limited for 2–3 monthsevery summer. Most ephemeral algae require about2–6 �M DIN for optimal growth (Fujita 1985; Fujitaand others 1989; Pedersen and Borum 1997). Nlimitation was therefore likely under ambient con-ditions in summer. The average background con-centrations of DIP were very low by northern Eu-ropean standards,—that is, always less than 1 �Mand below 0.2 �M for 4–5 months every year. Thelow DIP concentrations and high N:P ratios (morethan 160) observed in summer indicate that the

algae suffered substantial P limitation under ambi-ent conditions during most of the active growingseason. This conclusion is further supported by thehigh algal C:P ratios (circa 950), which are indica-tive of strong P limitation (Duarte 1992). Ambientnutrient concentrations were thus low enough torender the populations of microalgae and ephem-eral macroalgae nutrient-limited during most of thegrowing season. Nutrient enrichment was thereforeexpected to stimulate growth and hence the bio-mass of fast-growing algae in the mesocosms.

Nutrient-induced Stimulation of Growth

Nutrient enrichment did indeed stimulate thegrowth of ephemeral algae and periphyton, but thegrowth of more slow-growing filamentous red andperennial brown algae remained unaffected by theexperimental treatment. Nutrient enrichment stim-ulated the growth of ephemeral green algae duringthe summer months, when the background con-centrations of DIN and DIP were very low. Growthrates were enhanced by 10%–50%, depending ontreatment level; such an increase should lead to asignificant accumulation of biomass if loss rates re-mained constant. If, for example, the biomass ofgreen algae was 40 g DW m�2 and they grew at arate of 0.07 d�1 under ambient conditions, a 30%increase in growth rate would lead to an 100%increase in biomass within 1 month, provided thatlosses equaled production under ambient condi-tions and that they remained constant with nutri-ent enrichment. Periphyton grew significantlyfaster than green ephemeral macroalgae and wasstimulated for longer periods of time by nutrientenrichment. Considerable accumulation of per-iphyton was therefore also to be expected in re-sponse to nutrient enrichment unless periphytongrowth became severely reduced by self-shadingdue to high biomass or the loss rates increasedconsiderably at higher nutrient levels.

What are the mechanisms that prevented thefast-growing opportunistic algae from becoming thedominant species in the mesocosms? There are atleast three mechanisms that could have preventedthe recruitment and early development of opportu-nistic algae or imposed such massive losses on thesealgae that their biomass was kept low, even at thehighest nutrient loadings: (a) strong competition forspace and light imposed by the dense populations ofperennial canopy species. (b) strong top–down con-trol by herbivores, and (c) the physical disturbanceimposed by the wave machine and the subsequentexport of algal matter.

Table 3. Overall Mean Growth Rates of theMain Algal Components in the ControlMesocosms

Algal Component

Growth Rates (In units dN�1)

Mean Range CV

Periphyton 0.240 0.050–0.668 1.00Ulva lactuca 0.100 0.047–0.171 0.38Ceramium rubrum 0.105 0.061–0.172 0.47Fucus vesiculosus 0.041 0.017–0.072 0.61Fucus serratus 0.035 0.011–0.042 0.57

CV, coefficient of variationn � 60–84

588 T. L. Bokn and others

Competition from populations of perennial brown al-gae. It is well known that long-lived perennialbrown algae can build up dense canopies and sup-

press understory vegetation and attached epiphytesthrough heavy shading or “whiplash” effects (San-telices and Ojeda 1984; Kiirikki 1996). The popula-

Figure 7. Metabolism by algae in the mesocosms mea-sured by oxygen dynamics at different nutrient treatmentlevels through time. (A) Gross primary production (GPP).(B) Respiration (R). (C) Net primary production (NPP).

Figure 8. Relationships between the overall carbon–ni-trogen (C:N) and carbon–potassium (C:P) ratios of thealgal assemblages and nutrient treatment levels. Meanvalues � 1 SE (n � 6).

Table 4. Relationships Between Relative Response in Growth Rate and Nutrient Treatment Level amongPeriphyton and Four Species of Macroalgae

Algal Component Rspring Rsummer Rautumn

Periphyton R � 0.934(P � 0.001, n � 8)

R � 0,744(P � 0.001, n � 24)

R � 0.602(P � 0.014, n � 16)

Ulva lactuca R � N�0.103(P � 0.726, n � 14)

R � 0.635(P � 0.003, n � 20)

R �–0.425(P � 0.130, n � 14)

Ceramium rubrum R � 0.178(P � 0.543, n � 14)

R �–0.021(P � 0.931, n � 20)

R � 0.144(P � 0.503, n � 14)

Fucus vesiculosus R � 0.164(P � 0.575, n � 14)

R � 0.187(P � 0.418, n � 20)

R � 0.150(P � 0.608, n � 14)

Fucus serratus R � 0.114(P � 0.808, n � 7)

R � 0.284(P � 0.212, n � 21)

R � 0.254(P � 0.381, n � 14)

(R, correlation coefficients; P, probability; n, number Pearson correlation analysis for each main season

Response of Rocky Shore Communities to Nutrients 589

tions of perennial brown algae in the mesocosmswere very dense, and although we did not studycompetitive interactions directly, it is most likelythat they prevented the recruitment of ephemeralalgae. Ephemeral macroalgae and periphyton wererarely found below and upon fucoids in the densevegetation; they appeared almost entirely as epi-phytes on solitary fucoids or in gaps within theestablished vegetation.

Gaps (“free space”) appear whenever physicaldisturbance or age-related mortality detaches can-opy-forming individuals within the community.Such gaps are quickly colonized by ephemeral spe-cies, but these are often succeeded by slow-growingperennial algae (late-successional species, sensu Lit-tler and Littler 1980), which colonize and develop

more slowly but seem competitively superior in thelong run (see for example, Lubchenco 1983; Sousa1979). This successional sequence was evident inthe recruitment experiments conducted at low nu-trient concentrations, where clean granite tileswere colonized by all types of algae but becametotally dominated by perennial brown algae plusattached red algae within 1–2 years. However, gapscan remain dominated by ephemeral algae formuch longer if the availability of nutrients is highand/or the grazing pressure is low (Rueness 1973;Murray and Littler 1978; Sousa 1979), as seen inrecruitment studies carried out at high nutrientloading. Ephemeral green algae became completelydominant on these tiles and remained so for theentire course of the experiment, although theywere nearly absent from areas dominated by peren-nial algae within the same basins. Dense popula-tions of early colonizers thus seem able to preventthe settlement of spores from late-successional al-gae. Alternatively, adult stages of the ephemeralalgae may be competitively superior to the germ-lings of late-successional species as long as theirgrowth and biomass development are not restrictedby nutrient limitation or heavy grazing (Lubchenco1983; Worm and others 2001). Alternatively, theunsuccessful colonization by late-successional spe-cies at high nutrient concentrations may have beencaused by reduced reproductive output by fucoidalgae at high nutrient levels, but this possibility stillneeds to be tested.

The strong and persistent dominance of largecanopy-forming algae in all mesocosms, regardlessof treatment level, suggests that these algae canprevent, or delay, a massive accumulation ofephemeral algae when the availability of nutrientsincreases. Opportunistic algae appear, however, tohave the potential to establish competitive and per-sistent populations when free substrate becomesavailable under conditions of high nutrient richnessand low grazing pressure. It is therefore possiblethat ephemeral algae would have become muchmore dominant at higher treatment levels withtime, since age-driven mortality among the fucoidswill continue to create new gaps in the vegetation.Competitive replacement of late-successional algaeby opportunistic macroalgae with increased nutri-ent loading thus seems to be a slow process.

The effect of herbivory. Invertebrate grazers aretypically highly abundant in littoral communitiesdominated by large perennial algae and can atten-uate the primary effects of nutrient enrichment viaselective grazing on opportunistic algae (see, forexample, Lubchenco 1978; Geertz-Hansen and oth-ers 1993; Hauxwell and others 1998; Lotze and

Figure 9. Potential grazing pressure on (A) brown, (B)red, and (C) greenalgae across nutrient treatment levels.The potential grazing losses were estimated from species-specific consumption rates of the dominant herbivorescombined with the biomass of the same herbivores. Datawere available only for 1999 and 2000.

590 T. L. Bokn and others

others 2001; Nielsen 2001). Nutrient enrichmentmay also indirectly stimulate the abundance of her-bivores and hence the grazing pressure, becausefood of higher quality (that is, higher N and Pcontent) improves herbivore survival, growth, andreproduction (Mattson 1980).

Nutrient enrichment did improve food qualitysignificantly as the average C:P and C:N ratios of thealgae fell from 950 to 210 and from 19 to 11,respectively. However, the herbivore response wasnot clear, because the total abundance and biomassof herbivores remained largely unaffected by nutri-ent enrichment and only a few snails and smallcrustaceans became more abundant with highernutrient loading. The abundance of isopods andamphipods was highly variable and only weaklyrelated to nutrient enrichment, but the response ofthese free-swimming herbivores may have beenblurred by the significant export of individuals withthe outflowing water.

The small but important increase in the abun-dance of some herbivores with increasing nutrientenrichment resulted in a positive relationship be-tween total consumption and nutrient richness. Forall macroalgae, an increasing proportion of the pro-duction was consumed at higher nutrient richness,the response being strongest for red and brownalgae. The positive correlation shows that the her-bivore response was stronger than the response inalgal growth rate. The correlation was weak forephemeral green algae and inverse for periphyton,reflecting the fact that the growth rate of thesealgae was stimulated as much, as or more than, thegrazing losses.

The main herbivores (snails, isopods, and amphi-pods) preferred periphyton and ephemeral greenalgae to filamentous red algae and fucoids in the

“multiple choice” experiments carried out in themesocosms. Estimated consumption rates exceededthe production of periphyton and ephemeral greenalgae on an annual basis. The effect of grazing wasespecially strong during summer, when the herbi-vores were most abundant. The heavy grazing effectin summer is important because this is when op-portunistic algae showed the strongest response tonutrient enrichment. The massive consumption ofopportunistic algae indicates that the sustainedpresence of these algae in the mesocosms dependedon refuges in the mesocosm where they were inac-cessible to the herbivores due to physical or behav-ioral constraints.

The opportunistic algae were thus under strongtop–down control, even at the highest nutrient lev-els, and grazing is obviously one important mech-anism by which the primary effect of eutrophica-tion (that is, accumulations of periphyton andephemeral algae) was attenuated. These findingscontrast with those of Hauxwell and others (1998)and Lotze and others (2001), who found that thetop–down control on ephemeral macroalgae wasrelaxed with increasing nutrient enrichment be-cause growth rates were stimulated more than theabundance of herbivores. The role of herbivory thusseems to vary among systems and may depend onfactors such as the ratio between algal biomass orproduction and herbivore abundance. A decreasingimportance of herbivory with increasing nutrientrichness is obviously also possible if heavy eutrophi-cation is followed by events of anoxia and/or loss ofstructural habitats (that is, seagrasses, fucoids,kelps), which will reduce the abundance of fauna.

The role of physical disturbance and export. Physicaldisturbances created by wave exposure or strongtides can alter the structure of littoral communities

Table 5. Summary of Primary Production and its Fate in the Experimental Mesocosms

All Algae Brown Algae Red Algae Green Algae Periphyton

Gross primary productiona 2300–2350 — — — —Algal respirationa 1000 — — — —Net primary productionb 1300–1350 877 143 238 39Lost through grazingc 680 257 51 265 110Export of algal fragmentsd 210 42 42 115 ?Export of FPOC and DOCd 330 ? ? ? ?Not accounted fore 80–130 (578) (5) (–142) (–71)

FPOC, fine particulate carbon; DOC, dissolved organic carbon Means based on data from all eight mesocosms, 1999 data only Units given in g C mN�2 y N

�1aQuantified from measured oxygen dynamics combined with biomass data.bEstimated as the differences between gross primary production and respiration and quantified from algal growth measurements combined with biomass data.cEstimated from potential consumption rates by important herbivores and their abundance.dQuantified from samplings.eEstimated as the difference between net primary production and the sum of all accounted losses.

Response of Rocky Shore Communities to Nutrients 591

(Lubchenco 1980; Underwood and Jernakoff 1984;Phillips and others 1997) because delicate algae aremore sensitive to physical disturbance than large,leathery algae (Littler and Littler 1980). Physicaldisturbance and the subsequent export of detachedalgae may therefore help to prevent the heavy ac-cumulation of ephemeral algae, which would oth-erwise affect the perennial macrophytes negativelythrough dense shading.

The total export of large visible algal fragmentsfrom the mesocosms was rather small, representingonly 16% of the total production. However, theexport losses were not scaled to the biomass orproductivity of the different algal types since theephemeral green algae lost at least 56% of theirproduction through export. This number may evenhave been higher if the export of FPOC and DOCoriginating from these algae could have been in-cluded in the estimate. Although the export ofephemeral algae did not vary systematically withnutrient treatment, these losses—in addition to thegrazing losses—must have been significant factor inkeeping the standing biomass low.

Physical disturbance and the subsequent exportof detached algae may not play the same role inshallow and more sheltered estuaries and lagoons.Ephemeral algae may still be torn loose from theirsubstrate due to wave exposure or tides, but most ofthe detached algae will remain in the system asfree-floating macroalgae that can build up as “greentides” under the right conditions (Fletcher 1996;Raffaelli and others 1998).

The export of organic matter from the littoralzone of high production to neighboring systemsmay in some instances constitute an important in-put of matter and energy. If most of the exportedFPOC and DOC originated from algae, then thetotal export of algal matter would sum to 540 g Cm�2 y�1, corresponding to about 42% of the NPP.This number is comparable with the estimate ofDuarte and Cebrian (1996), who showed that sys-tems dominated by macroalgae exported, on aver-age, 44% of their NPP. Whether or not such anexport of organic matter is important for the recip-ient depends on the area of the receiving systemrelative to the littoral zone. If the area of the recip-ient is large relative to the littoral zone, as in mostexposed coastal areas or deep fjords, then the im-portance will be marginal. If, on the other hand, thearea of the recipient is small relative to the littoralzone, as in most lagoons and shallow estuaries, thenit may be substantial and support secondary pro-duction considerably.

SUMMARY AND CONCLUSIONS

A combination of strong competition from estab-lished stands of canopy-forming brown algae, im-mense herbivory, physical disturbance by waves,and the subsequent export of detached componentsall contributed to neutralizing the accumulation ofperiphyton and ephemeral macroalgae in the ex-perimental rocky shore ecosystems exposed to in-creased nutrient loading. This result suggests thatthe maintenance of ecosystem integrity, preservingan adequate cover by perennial species and associ-ated populations of mesograzers, is an essential re-quirement for maintaining healthy rocky shoreecosystems.

Natural rocky shore communities may, however,be more sensitive to nutrient loading than thisstudy suggests, because phytoplankton may be verysensitive to nutrient enrichment and add signifi-cantly to the light attenuation in the water columnunder natural conditions. Our results also suggestedthat the observed resilience against nutrient-drivenstructural changes among the primary producersmight not persist on a long time scale becauseephemeral algae are able to colonize free space andthus become dominant when nutrient richness ishigh and grazing pressure is low. These conditionswill probably appear sooner or later in any systemexposed to heavy nutrient loading since extremeevents (that is, storms, extremely cold winters orhot summers, ice-scouring, extraordinary low tides,and so on) will create gaps in the dense cover offucoids and/or reduce the abundance of herbivores.

ACKNOWLEDGEMENTS

This is contribution no. 401/11 of the ELOISE pro-gramme under the Research DG of the EuropeanCommission, of which the EULIT project (contractMAS3-CT97-0153) was part. The project was alsosupported by the MARICULT/Norsk Hydro Pro-gram. We thank Torgeir Bakke and Jon Knutzen fortheir valuable advice, and we are grateful to all ofthe participants in the project throughout the 5years of operation for their contribution. This paperis contribution no. 46 from the Marine ResearchStation, Solbergstrand, Norway.

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