Effects of Eutrophication, Grazing, and Algal Blooms on Rocky Shores
Author(s): Boris Worm and Heike K. Lotze
Source: Limnology and Oceanography, Vol. 51, No. 1, Part 2: Eutrophication of Freshwater
and Marine Ecosystems (Jan., 2006), pp. 569-579
Published by: American Society of Limnology and Oceanography
Stable URL: http://www.jstor.org/stable/4499611
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Limnol. Oceanogr., 51(1, part 2), 2006, 569-579
? 2006, by the American Society of Limnology and Oceanography,Inc.



Effects of eutrophication,grazing, and algal blooms on rocky shores
Boris Worm' and Heike K. Lotze
Biology Department, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada

        Abstract
                  can
          Eutrophication profoundly    changerockyshorecommunities.  Thesechangesoften cause the replacement  of
        perennial, canopy-forming  algae such as Fucusspp. with annual,bloom-forming algae such as Enteromorpha spp.
        Grazing, however, counteract
                   can      eutrophication eliminating annual
                                 by      the    algae'ssusceptible recruits. examine
                                                          We
        these generalizations  across large scales. We use replicated"bioassay"experiments comparethe effects of
                                                    to
        eutrophication grazingacrossfour pairedcontrolversuseutrophied
                 and                          sites in the Northwest Atlanticand four
        eutrophied in the BalticSea in springandsummer. each site, annual
              sites                    At         algalrecruitment grazingpressure
                                                      and
        were estimated  usingtiles seededwith Enteromorpha  intestinalis
                                         propagules.Tiles wereexposedfor 3 weekswith
        grazersexcludedor allowedaccess. Productivity E. intestinalis
                                  of       recruitswas stronglyrelatedto eutrophication
        (10-foldincrease)and grazing(80%decrease)and was weaklyrelatedto season.While the absolutegrazingrate
        increased a linearfashionwithalgalproductivity, relative
             in                    the        rate
                                       grazing remained         constant
                                                  surprisingly    (--80%).
        Comparative  field surveysshowedthatperennial  algae decreased 30-60%, while annualalgae, filterfeeders,
                                          by
        and grazersincreased  acrossa gradient eutrophication. eutrophication
                             of        As        increased from controlto eutrophied
        to pointsourcesites,rockyshorecommunities   becameincreasingly dominated singlespeciesof annualalgaeor
                                               by
        filterfeeders,and community   diversitydeclinedconsistently 24-46%. We concludethatgrazersareimportant
                                       by
        controllers algal blooms but that, ultimately,
              of                  they cannotoverridethe effects of increasing eutrophicationon
        rockyshorecommunity    structure biodiversity.
                          and


  Rocky shores are among the most dynamic and productive  such as propagules and recruits (Lotze and Worm 2000;
ecosystems on the planet. Biomass and primaryproductivity  Lotze et al. 2000). The interplay of eutrophicationand graz-
are typically dominated by canopy-forming perennial ma-   ing may thus determine the occurrence of algal blooms and,
croalgae such as fucoids and laminarians.Togetherwith sea-  on a larger scale, both structureand function of coastal eco-
grasses on soft-bottom habitats, these algae generate up to systems (Geertz-Hansen et al. 1993; Hauxwell et al. 1998;
40% of the primary productivity of the coastal zone (Char-  Worm et al. 2000).
py-Roubaud and Sournia 1990) and a significant fraction of   In this paper, we attempt to quantify and compare the
global marine plant biomass (Smith 1981). They also fulfill effects of eutrophicationand grazing across four paired con-
importantecosystem functions, including carbon storage, nu- trol versus eutrophied sites in the Northwest Atlantic and
trient cycling, and the provision of food and habitat for a four eutrophied sites in the Baltic Sea. Sites were selected
diverse invertebrateand fish fauna (Borg et al. 1997; Worm  on the basis of documented differences in nutrientstatus and
et al. 2000). Recently, perennial macroalgae and their asso-
                               eutrophication, and they represent a broad range of back-
ciated communities have severely declined in abundance in
                               ground conditions. Specifically, we were interested in dis-
regions such as the Baltic or the Adriatic Sea, where they  covering how annual algal recruitment,grazing pressure, and
have been replaced by few species of bloom-forming annual
                               community structure change with eutrophication. For ex-
algae (Vogt and Schramm 1991; Munda 1993). These       ample, it is an open question if grazing pressure is constant,
bloom-forming algae do not provide the same biogeochem-   increases, or decreases with increasing eutrophication.To an-
ical and habitat functions as perennial algae, and their massswer this question, we developed a simple grazer-nutrient
occurrence often has strong negative effects on coastal eco-
                               "bioassay" using tiles that were seeded with propagules of
systems and their inhabitants, including humans (Valiela et the bloom-forming green algae Enteromorpha intestinalis
al. 1997). Detailed observations and experiments have linked
                               and enclosed in open and closed cages. Detailed experimen-
the increased occurrence of annual algal blooms to elevated
                               tal evidence shows that a high abundance of E. intestinalis
nutrient loads from coastal eutrophication(Fong et al. 1993;
Hauxwell et al. 1998; Lotze et al. 2000). In addition, it hasis indicative of high nutrient supply, low grazing pressure,
been shown that grazers such as littorinid snails, isopods, or both. Especially early life stages of Enteromorpha spp.
and amphipods can reduce or even prevent algal blooms    (propagules and microscopic stages, hereaftercalled recruits)
                               are extremely responsive to changes in nutrientsand grazing
through selective feeding on their early life-history stages,
                               (Lotze and Worm 2000, 2002; Lotze et al. 2001). This sug-
  Correspondingauthor(bworm@dal.ca).            gests that E. intestinalis can be used as an indicatororganism
                               to assay changes in both eutrophicationand grazing pressure.
Acknowledgments                       In this study, we took advantage of this, using an experi-
  Specialthanksto InkaMilewskifor discussion,inspiration,
                             and mental design that allowed us to separatethe relative effects
                     and
field support; UlrichSommer comments suggestions;
       to       for             and
to WadeBlanchard statistical
         for     advice.This workwas supported and potential interactions between eutrophication and graz-
by the GermanMinistryof Science and Education, German ing. As a further advantage, E. intestinalis thrives under a
                         the
ResearchCouncil(DFG), and the Conservation Councilof New  wide range of salinity, temperature, and light conditions
Brunswick (CCNB).                      (Woodhead and Moss 1975; Reed and Russell 1979), which
                                   569
570                                 Wormand Lotze


                 A          1000'         B        -66 00'        -64 00'
            55 00'                                                      46 00'

                 Flensb
                                           St.  John
                                                    61
            54  45'
                               Baltic        LI                          45 00'
                                Sea                       Ha

            54 30'
                  Eckernfoerde44                                             00'
                                       KF          'Atlantic '
            54 15'

                                                                ~    43 00'
         C,              S...
                  C                  D                    E
            45 10'   1                                                  44 45'

                    U       c4          Fundy




                           Bayofof
                           Fundy                                Atlantic
                                                  4430'
                                                    2Ocean
                      -67 00'     -66 45         -65 45'      -65 30 -6340'      -63 30'
                                      Longitude (E)
           Fig. 1. Locations of experimental and survey sites in the (A) Western Baltic Sea and (B) North-
         west Atlantic. See Table 1 for site code definitions. Open squares represent individual sites, and
         black squares represent major cities. Location of eutrophied (EU), control (CO), and point source
         (PS) sites within PB: Passamaquoddy Bay and LI: Letang Inlet (C), AB: Annapolis Basin (D), and
         HH: Halifax Harbor (E) are shown. Experiments and surveys were conducted at all EU and CO
         sites in spring and summer; PS sites were surveyed in spring only.



facilitates comparisons across different sites. In addition to          1996b), which drains the largest agricultural area in the prov-
field experiments, we performed comparative field surveys            ince and was the first of these sites to be settled by Euro-
across all sites to test how rocky shore community structure           peans in 1605. LI and PB have been affected since about
changes with eutrophication and how the abundances of pe-            1800 by logging, pulp mills, sewage, and fish processing,
rennial and annual algae, benthic filter feeders, grazers, and          and since 1980, they have harbored some of the highest con-
predators covary.                                centrations of salmon aquaculture farms in North America
                                         (Lotze and Milewski 2004). Recently, these four embay-
Methods                                     ments were monitored by government agencies to document
                                         the extent of ongoing nutrient pollution and eutrophication
  Study sites-To  study the effects of anthropogenic eutro-          from sewage, agricultural runoff, and aquaculture. Within
phication, we selected a total of 16 sites in the Northwest           each region, one control and one eutrophied site were estab-
Atlantic and the Western Baltic Sea (Fig. 1). In the North-           lished on the basis of published long-term monitoring data
west Atlantic, four large embayments in Nova Scotia (Hal-            of dissolved nutrient and suspended chlorophyll a (Chl a)
ifax Harbor [HH] and Annapolis Basin [AB]) and New                concentrations (Fig. IC-E; Table 1) (data compiled from
Brunswick (Letang Inlet [LI] and Passamaquoddy Bay [PB])             Dalziel et al. 1991; Keizer et al. 1996a,b; Strain and Clement
were chosen as study regions (Fig. 1B). Each of these re-             1996; and the database of the phytoplankton monitoring
gions has been settled by Europeans for >200 yr and has             group, Bedford Institute of Oceanography, Dartmouth, Nova
received large amounts of anthropogenic nutrient and organ-           Scotia, Canada). While all eutrophied sites in the Northwest
ic inputs. Since its settlement in 1749, HH (Fig. lE) has            Atlantic showed elevated nutrient and chlorophyll concen-
received untreated municipal sewage from up to 250,000              trations compared with their respective control sites, back-
people (Dalziel et al. 1991). AB receives large amounts of            ground nutrient concentrations varied widely and overlapped
agricultural runoff from the Annapolis River (Keizer et al.           among eutrophied and control sites of different regions (Ta-
                       Eutrophication and rocky shores                       571


  Table1. Experimental in the Northwest
           sites       Atlantic(HH-PB)andBalticSea (FF-GB). Dissolvedinorganic
                                                nitrogen(DIN),dissolved
inorganic     (DIP),and chlorophyll averages(May-Aug)were derivedfrompublished
     phosphorus          a                       monitoringsources;watertemperature
(Tspng: May-Jun,  Jul-Aug)and salinity(May-Aug)were measureddirectly.ND, no data.
        T...e,:
                            DIN    DIP    Chla       Tspring   Tsummer
     Region      Code    Eutrophication (AmolL-') (tkmolL-1) (jig L-')      (oC)    (oC)   Salinity
HalifaxHarbor        HH     Control     0.44   0.34   0.55       10.7    16.8    30.1
HalifaxHarbor        HH     Eutrophied    0.78   0.81    1.15       8.4    18.4    30.1
Annapolis Basin       AB     Control     4.84   0.45   2.28        9.7    13.5    31.8
Annapolis Basin       AB     Eutrophied    6.00   0.75   3.50       12.4    17.7    30.0
LetangInlet         LI     Control     7.28   0.90    1.69       10.0    16.0    30.7
LetangInlet         LI     Eutrophied   13.29   1.14   2.10        8.7    16.1    31.0
Passamaquoddy Bay     PB     Control     4.84   0.45    ND        9.4    15.1    30.8
Passamaquoddy Bay     PB     Eutrophied    5.97   0.62    ND        11.3    16.5    30.2
Flensburg Fjord       FF     Eutrophied    1.14   0.93   2.10       13.1    15.4    15.8
Schlei Fjord        SF     Eutrophied    1.35   0.23   6.71       16.1    18.8    14.5
Kiel Fjord         KF     Eutrophied    3.04   4.52   9.84       14.0    16.2    15.1
GeltingBay         GB     Eutrophied    ND    ND    ND        16.0    19.0    15.9



ble 1). This was because the Bay of Fundy (AB, LI, and PB    immersed in freshly collected seawater (80C) with tiles un-
sites) (Fig. IC,D) features strong tidal mixing and regional   derneath and exposed to natural daylight and temperatures
upwelling, whereas HH sites (Fig. 1E) receive nutrient-poor   around 15TC.This initiated the release and fertilization of
offshore waters (Keizer et al 1996a,b). We took into account   propagules, which were allowed to settle on tiles for 30 h.
these differences when designing the study, since it was our   Seeded tiles were stored for 1-2 d in filtered seawater in the
goal to analyze the effects of anthropogenic eutrophication   dark at 100C until they were used in the experiment. During
across a broad range of background conditions. We further    each experimental run, five tiles were cultivated in the lab-
sampled four point source sites in spring that were located   oratory to quantify the initial settlement density of E. intes-
near (0.5-2 km) sewage outfalls (HH and AB) (Fig. 1D,E),     tinalis propagules on the tiles. Each tile was placed in 500
a fish processing plant (LI) (Fig. 1C), and salmon aquacul-   ml of filtered and nutrient-enriched seawater (Provasoli
ture operations (PB) (Fig. IC). This was done to see whether   1965) and cultured for 23 d at 100C and 100 jimol photons
community changes observed at eutrophied versus control     m-2 s-1 in a 14:10 light: dark cycle.
sites increase in magnitude near a nutrient point source.      For the field experiment, tiles were enclosed in circular
  In the Baltic Sea, four fjordlike embayments were chosen   cages (closed cages: "No Grazer"; open cages: "Grazer"
as study regions, and one eutrophied study site was estab-    treatments) or exposed on uncaged control plots ("Grazer
lished in each (Fig. lA; Table 1). These sites had high nu-   Control" treatments).We ran five replicates per treatmentat
trient loading typical of inshore regions in the Baltic Sea.   each of 12 sites during spring and summer, giving a total of
Control sites could not be established, as the whole Western   24 individual experiments (Fig. 1). Cages were mesh bags
Baltic suffers from the strong influence of anthropogeniceu-   (15 X 15 cm) made from a clear polyethylene mesh with 1-
trophication (Vogt and Schramm 1991). Nutrient and chlo-     mm openings. Bags were closed at one end. The open end
rophyll data (Table 1) were compiled from Schramm et al.     was fixed across an 8-cm-diameterpolypropylene base made
(1996), Hillebrand(1999), Worm et al. (2000), and the coast-   from sanitarytubing ends. A strong rubberring (4-mm thick-
al resource data base of the State Department for the Envi-   ness) sealed the cage against the base. "Grazer" treatments
ronment (Landesamtfiir Natur und Umwelt, Kiel, Germany).     had two 4.5- X 4.5-cm openings to provide access to grazers.
To compare hydrographicconditions among sites, water tem-    In the Northwest Atlantic, cages were placed in the Fucus
peratureand salinity at 1-m depth were recorded every time    vesiculosus zone, which spans the lower to mid-intertidal.
the sites were visited (Table 1).                The chosen shore level corresponded to approximately 8-9
                                 h of immersion per tidal cycle. Cages and uncaged tiles were
 Field experiments-Grazer-exclusion experiments were      fastened on sloping intertidal shorelines with 4-cm wedge
conducted at four eutrophied sites in the Baltic (Fig. lA)    anchors inserted into holes that were drilled with a gasoline-
and at four paired eutrophied and control sites in the North-  powered hammer drill. In the Baltic Sea, cages were also
west Atlantic (Fig. 1B-E) in spring and summer 1998 and     placed in the F. vesiculosus zone located between 0.6- and
1999, respectively. Point source sites were not included in   0.9-m water depth and were secured with two tent picks.
these experiments. At each site, annual algal recruitment      Tiles were exposed for 23 d at the experimental sites (Bal-
with and without grazers was quantified by exposing tiles    tic, 3-26 May and 6-29 July 1998; Northwest Atlantic, 16
seeded with E. intestinalis propagules in replicated cage ex-  May-8 June and 2-25 August 1999) and were then collected
periments. First, heat-sterilized, unglazed ceramic tiles (5 X  and analyzed in the laboratory.The later timing in the North-
5 cm) were seeded with 1 kg of fertile E. intestinalis thalli  west Atlantic corresponded to the later onset of spring and
collected at the experimental sites. The algae were dripped   the slower warming of the water column in this region. In
dry and stored overnight in the dark at 80C. Thalli were then  the laboratory,we estimated E. intestinalis recruit density at
572                          Wormand Lotze


x25 magnification under a dissecting microscope. E. intes-    Results
tinalis recruits were counted in 10 random 4- x 4-mm sub-
samples per tile. Other macroalgal recruits were rare and      Field experiments-Cultivation of experimental tiles in
were not quantified. E. intestinalis recruit density was av-   the laboratory showed that the seeding procedure was suc-
eraged from subsamples to a 1-cm2 area for all experimental   cessful. E. intestinalis propagules settled densely on the tiles
tiles. E. intestinalis productivity was calculated as the per-
                                 (2,210 + 308 cm-2, mean ? 1 SE, n = 20), and densities
centage of recruits that developed from settled propagules to  were not significantly different among the four runs of the
germlings in the absence of grazing (settlement density was   experiment (ANOVA, F3,16 = 2.5, p = 0.098). These den-
determined in the laboratory, see above). Grazing rate was    sities are representativeof daily settlement of E. intestinalis
calculated as the percentage of recruits that were lost in
                                 propagules on ceramic tiles in the Baltic (1,000-6,000 cm-2
"Grazer" relative to "No Grazer" treatments.           d-' from May to August) (Lotze et al. 2000).
                                  In the field, only a fraction of settled propagules devel-
  Field surveys-Detailed field surveys were conducted at    oped into recruits. Averaged across all experiments, recruit
all 16 control, eutrophied, and point source sites during the  density after 23 d in the field was 174 + 25 cm-2 (range =
spring experiments. At each site, 10 replicate frames (50 X   0-2,665, n = 259), or 8% of settled propagules. E. intestin-
50 cm) were placed randomly along 100-150-m transects at     alis recruit density was strongly controlled by eutrophica-
the experimental shore level (corresponding to the F. vesi-   tion, with a 10-fold increase between control and eutrophied
culosus zone, see "Field experiments"). Percentage covers    sites (Fig. 2). Eutrophied sites in the Atlantic were signifi-
of attached algae and sessile invertebrateswere determined    cantly different from control sites (Tukey test, p < 0.05) but
by species using a Plexiglas frame with 50 random points.    were not significantly different from eutrophied Baltic sites.
We sampled epiphyte cover, secondary space cover, and pri-     Grazers also had strong and consistent effects on E. in-
mary space (understory) cover. The latter was determined     testinalis, causing an 80% decrease between "No Grazer"
after removing the fucoid canopy from the sample plots.     and "Grazer" treatments (Fig. 2). "No Grazer" treatments
Grazers and predators were removed by shaking the algae     were significantly different from both "Grazer" as well as
within a framed sampling net and were counted by species     "Grazer Control" treatments.There were no detectable cage
(except for gammarids, which could not be identified reli-    artifacts (Tukey's test "Grazer" vs. "Grazer Control," p >
ably). Species richness was calculated from these data. In    0.2). Although both effects were statistically significant, eu-
the Northwest Atlantic, the four control and four eutrophied   trophication explained about twice as much of the variance
sites were resampledfor species richness in summer to check   as grazing (Table 2). No significant interaction between eu-
whether patterns in spring were representative.         trophication and grazing was detected, suggesting that their
                                 effects were largely independent.
                                  The effect of season was marginally nonsignificant (p =
  Data analysis-For analysis, we pooled all replicates
                                 0.052) and explained less than half of the variance compared
within each site, as "site" was considered the appropriate    with grazing and less than one fourth compared with eutro-
experimental unit in this comparative study. We analyzed E.   phication (Table 2). In spring, relative grazing effects were
intestinalis recruit density on the experimental tiles as a
                                 consistently strong in the Baltic and the Northwest Atlantic
function of eutrophication("Control Northwest Atlantic" vs.
                                 (Fig. 2A). In summer, grazing effects became more variable
"EutrophiedNorthwest Atlantic" vs. "EutrophiedBaltic"),     overall (Fig. 2B), and grazing control of annual algal re-
grazer presence ("Grazer" vs. "No Grazer" vs. "Grazer      cruitmentvanished entirely at two sites in the Baltic (SF and
Control"), and season (spring vs. summer) using factorial    GB) (Fig. 2B). Across all sites, recruit density without graz-
fixed-factor analysis of variance (ANOVA). Data were log     ers was higher in spring (346 ? 131 cm-2) than in summer
transformedto achieve homogeneity of variances tested by     (201 ? 139 cm-2), and recruit density with grazers was low-
the Cochran test. The Tukey post hoc test was applied to     er in spring (75 ? 49 cm-2) than in summer (92 ? 58 cm-2).
compare different treatment levels. The variance explained    This may indicate higher nutrient supply and grazing pres-
by each factor was calculated as  SSfactor,/SStota1       sure in spring and lower nutrientsupply and grazing pressure
  For the field surveys, we used analysis of covariance (AN-  in summer.
COVA) to analyze cover of perennial algae, annual algae,       Overall, there was a highly significant log-linear relation-
filter feeders, grazers, and predators as a function of eutro-  ship between recruit densities in "Grazer" and "No Grazer"
phication ("Control Northwest Atlantic" vs. "Eutrophied     treatments (Fig. 3A), indicating surprisingly consistent ef-
Northwest Atlantic" vs. "Point Source Northwest Atlantic"    fects of grazing across several orders of magnitude in E.
vs. "Eutrophied Baltic"). We included the abundance of      intestinalis density (this excludes two Baltic sites where
consumers (grazers for algae and predatorsfor filter feeders   grazing broke down in the summer). The regression line was
and grazers) and resources (annual algae for grazers and fil-  significantly different from the 1: 1 line (t = -3.8425, p =
ter feeders for predators) as covariates, in order to account  0.0011), and the mean treatment effect was an 80% reduc-
for site-specific differences in the variables. Percent cover  tion in E. intestinalis density due to grazing. There was no
data were angular (arcsine-square root) transformed, and     linear trend of relative grazing rate with increasing E. intes-
grazer and predator data were log transformed to achieve     tinalis productivity, though grazer effects became more var-
homogeneity of variances.                    iable as E. intestinalis productivity increased (Fig. 3B).
                             Eutrophication and rocky shores                       573


            10,000      A) Spring

                           [ ]No Grazer
             1,000            *Grazer

               100


               10
                       0.9
                       ? .3
          7Z       1

           2 10,000
                     B) Summer

             1,000


               100-


               10
                                      0.1        no
                                      ?0.        data
                 HH AB LI PB          HH AB LI PB       FF SF KF GB
                      Control          Eutrophied        Eutrophied
                     NW Atlantic         NW Atlantic        BalticSea
           Fig. 2. Field experiments.Effectsof eutrophication grazingon recruit
                                     and        densitiesof the green
          alga Enteromorpha  intestinalisat 12 sites in the NorthwestAtlanticand Baltic Sea. (A) Spring
          experiment. Summer
                (B)      experiment. Data are mean ? 1 SE (n = 5). Grazer controltreatments
          werenot significantly differentfromcagedgrazer  treatments arenot shown.Foranalysis,
                                       and              refer
          to Table2.



  Field surveys-Surveys at the 12 experimental sites and         (F. vesiculosus, Ascophyllum nodosum), and annual algae
four point source sites (see Fig. 1) showed trends of decreas-      were mostly ulvoids (e.g., E. intestinalis, Ulva lactuca) or
ing cover of perennial algae and increasing annual algae,         ectocarpoids (e.g., Pilayella littoralis, Ectocarpus spp.). Fil-
filter feeders, grazers, and predatorswith eutrophication(Fig.      ter feeders were mostly mussels (Mytilus edulis, Mytilus
4). There was, however, considerable variability among sites,       trossulus) and barnacles (Balanus crenatus, Balanus im-
and not all trends were statistically significant (Table 3). Bal-     provisus). Grazers were mostly gastropods (e.g., Littorina
tic sites showed on average higher annual algal cover and         littorea, Littorina saxatilis), isopods (e.g., Idotea baltica,
higher grazer densities than Northwest Atlantic sites but low-      Idotea chelipes), or amphipods (Gammarusoceanicus, Gam-
er perennial algal cover. Perennial algae were mostly fucoids       marus locusta). Predatorswere mostly starfish (Asterias vul-
                                     garis), whelks (Nucella lapillus), and crabs (Carcinus maen-
 Table2. ANOVA.Effectsof eutrophication,                 as). Negative trends with eutrophicationwere significant for
                      grazing, season
                          and
on Enteromorpha intestinalisrecruitdensity in the field experi-      perennial algae, and positive trends were significant for graz-
ments.Datawere (log + 1) transformed. meansquare.
                   MS,                 ers and marginally nonsignificant for annual algae (Table 3).
                                     In addition to eutrophication,grazer density (as a covariable)
                                     explained much of the variance in annual algal cover. This
    Source      df       MS   F    p   variance  means that algal blooms typically occurred at those eutro-
       (E)
Eutrophication      2       4.1   8.3  0.0007  19.0   phied sites that had low grazer densities, namely eutrophied
Grazing(G)        2       2.1   4.3  0.0192   9.7   sites HH, LI, FF, KF, GB, and point source site PB (Fig. 4).
Season(S)        1       1.9   4.0  0.0522   4.5   Predator density was a significant covariate for both filter
EXG           4       0.0   0.1  0.9903   0.3   feeder and grazer abundance, which may indicate significant
EXS           2       1.0   2.0  0.1435   4.6   effects of secondary consumers. Grazer abundance was also
Gx S           2       0.4   0.9  0.4061   2.1   significantly related to annual algal cover, which may indi-
Ex G x S         4       0.2   0.4  0.8052   1.8   cate simultaneousresource control of grazerpopulations (Ta-
Residuals        51       0.5
                                     ble 3). Eutrophicationand consumer-resourcecovariates ex-
574                           Worm and Lotze


   1000                             Discussion

                                    This study suggests that eutrophication and grazing are
    100-                             key variables that explain much of the patternsand processes
                                  on rocky shores subject to anthropogenic influences.
                                  Throughout our experiments, eutrophication increased the
     10                            productivity of bloom-forming green algae, which are nor-
                                  mally kept in check by grazing. We found surprisingly con-
                                  stant effects of grazing across several orders of magnitude
  o    1    4                        in algal productivity. While the absolute number of recruits
                R2= 0.833, p<0.0001         removed increased in a linear fashion with E. intestinalis
                                  productivity (Fig. 3A), the relative grazing pressure re-
  o 0.1                              mained constant at about 80% on average (Fig. 3B). Thus,
 d      1     10    100     1000 10000
                                  grazers are important controllers of algal blooms, but ulti-
        Recruit density (cm-2)    - No grazer      mately, they cannot override the effects of increasing eutro-
                                  phication. The apparentconstancy of grazing effects may be
     120                            explained by the functional response of the main grazer spe-
        B                          cies, the gastropods L. littorea and L. saxatilis. Sommer
     100
                    *        *      (1999) found that L. littorea ingestion rates for benthic mi-
     80 -;                           croalgal films increased with algal biomass in a saturating
  o                                function. At subsaturatingfood levels, L. littorea increased
     60                            the area grazed per time but not the grazing intensity in that
                                  area. The grazing rates we found may thus correspondto the
     40                            average area that is grazed, not the grazing intensity per area.
  N
                                    Using E. intestinalis propagules as a grazer-nutrient"bio-
     20          R2= 0.045, p=0.36          assay" proved successful in our experiments. E. intestinalis
                                  responds quickly to changes in nutrient supply and grazing
      0            ,               pressure and thrives under a wide range of environmental
       0.1       1       10      100   conditions (Woodhead and Moss 1975; Reed and Russell
                                  1979; Lotze and Worm 2002). Thus, this simple methodol-
              Productivity   (%)          ogy could be a useful tool to compare and monitor biological
  Fig. 3. Grazingand Enteromorpha   intestinalis
                         productivity.(A) processes across many sites and to assess eutrophicationsta-
Densitiesof E. intestinalisrecruits experimental
                 in        "Grazer" versus tus across a wide range of environments. Similar "grazer
"No Grazer"  treatments followeda stronglinearrelationship.  (B) assays" were used on coral reefs (Hay et al. 1983) and rocky
             of
Grazing (percentage recruits
     rate           removed)  showedno trend with shores to quantify spatiotemporalgradients in grazing pres-
E. intestinalisproductivity        of
               (percentage settledpropagules   that sure (Worm and Chapman 1998). These previous experi-
recruited the absenceof grazing)acrossall field experiments. ments showed that grazing
      in
                                                 pressure varied predictably with
Pointsrepresent meansof five replicates site.
                     per            water depth and time of day (coral reef) and shore height
                                  and season (rocky shore), respectively. In our experiments,
                                  grazing pressure was surprisingly constant across sites and
                                  seasons but became more variable in summer (Fig. 2B) and
plained 48-93% of the variance in abundance of these
functional groups (Table 3). In addition, there was a positive   at high levels of E. intestinalis productivity (Fig. 3B). In the
trend for annual algae (R2 = 0.26, p = 0.088) and a negative    Baltic Sea, grazereffects were strong in spring but weakened
trend for perennial algae (R2 = 0.27, p = 0.083) with E.      considerably in summer (Fig. 2). This pattern was also seen
intestinalis productivity as measured in the experiments. Fil-   in previous field experiments and linked to increasing pred-
ter feeder abundancewas strongly positively correlatedwith     ator abundance and consumer control of grazer populations
Chl a concentrations (R2 = 0.71, p = 0.0044), as derived      in the summer months (Worm et al. 2000). E. intestinalis
from published long-term monitoring sources (Table 1).       recruitment in the absence of grazing was lower in summer
  Changes in community structurewith eutrophication led      than in spring in both oceans. This probably indicates in-
to declining species richness (Fig. 5; Table 3). Richness de-    creasing nutrientlimitation of bloom-forming green algae in
clined by 24% with eutrophicationin the Northwest Atlantic     summer (Pedersen and Borum 1996). Although we cannot
and by 46% at sites that were close to a nutrientpoint source.   exclude high temperatureor other limiting factors that may
Species loss with eutrophication was most pronounced in       vary seasonally, patterns of increasing nutrient limitation,
perennial algae, followed by annual algae, grazers,predators, decreasing algal biomass, and decreasing grazing pressure
and filter feeders. Declines in species richness between      from spring to summer have also generally been found in
Northwest Atlantic control and eutrophied sites were con-      phytoplanktoncommunities (Sommer et al. 1986).
sistent in spring and summer (Fig. 5) (ANOVA, eutrophi-        In accordance with the experimental results, our field sur-
cation [E] F,,,, = 4.5, p = 0.056, season [S]       = 0.2, p veys showed that massive blooms of annual algae typically
= 0.698, E X S      = 0.1, p = 0.807).     F11,l      occurred at eutrophied sites with reduced grazer densities.
          F,,l,
                           Eutrophication and rocky shores                     575


                120 A) Perennial
                       algae
                100
                80-
                o
                60-
                S
                40-
                20

                   B) Annualalgae
                100-
            >    80 -
                60




                   C) Filterfeeder
                60-

                40-

                2
                20


                   D) Grazer
               2000
               1500

              S1000

               500


                   E) Predators
                40-

            'i   30 -
                20 -

                10-        101        Lno                 data
                    HH AB LI PB Mean HH AB LI PB Mean HH AB LI PB Mean FF SF KF GB Mean
                    Control       Eutrophied  Eutrophied
                                          (PS)      Eutrophied
                    NW Atlantic     NW Atlantic   NW Atlantic      BalticSea
           Fig. 4. Field surveys. Four control sites are contrasted with four eutrophied sites and four point
         source (PS) sites in the Northwest Atlantic, as well as four eutrophiedsites in the Baltic Sea. White
         bars represent means of 10 replicates per site (+1 SE), and black bars representmeans across four
         sites (+ 1 SE). For analysis, refer to Table 3.


The data in Fig. 4 suggest that blooms are likely to occur at     intense macroalgal blooms (Geertz-Hansen et al. 1993;
<500 grazers m-2 in the Baltic and at <100 grazers m-2 at       Hauxwell et al. 1998; Lotze et al. 2000). Field surveys also
eutrophied Northwest Atlantic sites; the cause for this dif-     showed that perennial algae declined between 30% and 60%
ference is speculative. This corroborates the results of pre-     in abundance with eutrophication. This is likely linked to
vious experiments showing that increased nutrient loading       interference with annual algae, which block perennial re-
and reduced grazer densities are both conditions that favor      cruitment, as demonstratedby previous field experiments in
576                          Worm Lotze
                              and

          Table3. ANCOVA.Effectsof eutrophication (maineffect) and consumer resourceabun-
                                           and
         dance(covariates) rocky shorecommunities.
                 on           Coverdatawere angular  transformed, abun-
                                              and
         dancedatawere log transformed. meansquare.
                       MS,


           Dependent       Source      df  MS    F    p   variance
         Perennial
             algae     Eutrophication    3   0.35  4.7  0.0240  56.0
                    Grazer        1   0.00  0.1  0.8194   0.2
                    Residuals      11   0.07
         Annualalgae      Eutrophication    3   0.13  3.0  0.0761  19.8
                    Grazer        1   1.09  25.6  0.0004  56.1
                    Residuals      11   0.04
         Filterfeeder     Eutrophication    3   0.05  2.1  0.1768  32.1
                    Predators       1   0.13  5.4  0.0485  27.4
                    Residuals       8   0.02
         Grazer        Eutrophication    3   0.28  15.2  0.0019  43.7
                    Annualalgae      1   0.73  39.1  0.0004  37.5
                    Predators       1   0.23  12.5  0.0095  12.0
                    Residuals       7   0.02
         Predators       Eutrophication    3   0.18  0.6  0.6196  12.2
                    Filterfeeder     1   1.54  5.4  0.0485  35.4
                    Residuals       8   0.29
         Speciesrichness    Eutrophication    3  83.4   5.7  0.0115  58.8
                    Residuals      12  14.6



the Baltic Sea (Worm et al. 1999, 2000). Annual algae and
grazers on average increased with eutrophication,as did fil-
ter feeders and predators on some sites (Fig. 4). However,
increased abundanceof some generalist species with increas-
ing eutrophication was accompanied by declining species
richness across all groups, most notably in the algae (Fig.
5). Thus, eutrophication may shift the competitive balance,
such that few species can monopolize abundant resources,
leading to a marked decline in diversity. Similar declines in
diversity were caused by experimental eutrophication (and

   25
                      Spring
   20-                [F Summer

-   15-

  S10

    5-

    0
     Control   EutrophiedEutrophied  (PS) Eutrophied
    NW Atlantic NW Atlantic NW Atlantic BalticSea
 Fig. 5. Diversity eutrophication rockyshores.Totalspecies
          and       at
richnessof benthicmacrophytes invertebrates sampledin
                and        was
the Northwest Atlanticat four controlsites, four eutrophied
                             sites,
fourpointsource(PS) sites, andfoureutrophied in the Baltic.
                        sites
Dataare mean 1 1 SE (n = 4). For analysis,referto Table3.
                       Eutrophication and rocky shores                       577



         Predators                                  Predators
          * whelks     '**"
                                                  * fish
          * starfish       "*                          *shrimps


          Filter feeder                                Grazer
            *
            mussels                                * gastropods
                                       .**.*
           *barnacles                    .a*            isopods



         Phytoplankton          Perennial canopy-          Annual bloom-
                          forming algae           forming algae
            *diatoms             * fucales             * ulvales
          odinoflagellates         * laminariales           *ectocarpales


                             Nutrients



                aV




 Fig. 6. (A) Food web interactions (B-D) alternative
                  and        community  stateson rockyshores.Upward  arrowsindicateresource ("bottom-
up") effects, and downward  arrowsindicateconsumer("top-down")effects. Dotted arrowsindicateindirectpositive effects. Nutrient
enrichment stimulates growthof phytoplankton indirectly
           the            (and     filterfeeders)as well as annualbloom-forming algae over the growth
of perennial algae. Predators grazerslimit the growthof filterfeedersand annualalgae and may indirectly
               and                                    maintain perennial algae.
Excessiveeutrophication override
            can     top-downcontrolandfavorthe development (B) musselbeds or (D) annualalgae,bothof which
                                       of
displace(C) perennial algal canopies.

stone" predators are classic patterns in community ecology    consistent with observations and experiments in Oregon
(Fig. 6A) (Paine 1966; Lubchenco and Menge 1978). How-      (Menge et al. 1997) and New Zealand (Menge et al. 1999),
ever, there is increasing evidence that nutrient supply can    indicating higher filter feeder and predatordensity and higher
overrunthis powerful interaction.Nutrient-richconditions fa-   predationrates at nutrient-enriched  sites.
vor phytoplanktongrowth and, indirectly,filter feeders, which    In conclusion, comparative experiments and observations
can then escape predatorcontrol and begin to dominate the     in the Baltic and Northwest Atlantic indicate that community
substratum (Menge et al. 1997, 1999). Our field surveys      structureon rocky shores is controlled and maintained both
showed that filter feeders increased strongly at some eutro-   by nutrient supply and consumer pressure (Fig. 6A). While
phied sites. All eutrophied sites had elevated Chl a concen-   grazers and predators control their prey under normal con-
trationscomparedwith their respective control sites, and there  ditions, increased nutrient supply can change the interaction
was a strong positive correlation between Chl a and filter    from predominantconsumer control to predominantresource
feeder abundance. Furthermore, the density of predators      control. This can lead to the replacement of perennial algal
(mostly starfish,whelks, and crabs) was positively related to   canopies (Fig. 6C) either to mussel beds (Fig. 6B) or annual
filter feeder abundance,which may indicate the transmission    algal blooms (Fig. 6D) and to marked declines in community
of bottom-upeffects to higher trophic levels. These results are  diversity. Whether these alternative community states on
578                            Wormand Lotze


rocky shores are stabilized by positive feedbacks and are         ecological controls on macroalgal recruitment.Limnol. Ocean-
therefore difficult to reverse is an important question that           47: 1734-1741.
                                   S ogr.
remains to be tested experimentally (Scheffer and Carpenter         ,     , AND U. SOMMER.2000. Propagule banks, herbiv-
2003). On the positive side, recent field surveys indicate the      ory and nutrient supply control population development and
                                     dominance patterns in macroalgal blooms. Oikos 85: 46-58.
recovery of F. vesiculosus populations and associated fauna
in the Baltic Sea following the reduction of nutrient loads         --,    , AND    . 2001. Strong bottom-up and top-
                                     down control of early life stages of macroalgae. Limnol.
(Nilsson et al. 2004; Worm pers. comm.). This may be in-         Oceanogr. 46: 749-757.
terpreted as a hopeful sign that wise management actions       LUBCHENCO, J., AND B. A. MENGE. 1978. Community development
can reverse the deleterious trends discussed in this paper,        and persistence in a low rocky intertidal zone. Ecol. Monogr.
even over large spatial scales.                      48: 67-94.
                                   MENGE, A., B. A. DALEY,P. A. WHEELER, DAHLHOFF,
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