KELP PATCH DYNAMICS IN THE FACE OF INTENSE HERBIVORY: STABILITYOF AGARUM CLATHRATUM (PHAEOPHYTA) STANDS AND ASSOCIATED FLORA

ON URCHIN BARRENS1

Patrick Gagnon,2 Ladd E. Johnson,3 and John H. Himmelman

Departement de biologie & Quebec-Ocean, Universite Laval, Quebec, Quebec, Canada, G1K 7P4

The brown alga Agarum clathratum (Dumortier)is the only large, perennial, fleshy macrophyte com-monly found on urchin-dominated barrens in thenorthwestern North Atlantic. We examined the spa-tial and temporal stability of A. clathratum standsand their impact on algal recruitment in the MinganIslands, northern Gulf of St. Lawrence. The standswere highly stable in space and time, with onlysmall intersite variations. The percent cover ofA. clathratum in 144-m2 areas increased by 6.5%–11.4% over a 2-year period, and most changes inabundance occurred at the edge of the stands. Thesurface area of small (o13 m2) single stands ofA. clathratum increased by approximately 1.8% .month� 1, although marked increases (495%) oc-curred during winter, largely because adjacentstands merged into larger single stands. Maturestands of A. clathratum appear to enhance algal re-cruitment, as juvenile A. clathratum and the under-story red alga Ptilota serrata (Kutzing) were ordersof magnitude more abundant inside than outsidethe stands. The experimental removal of theA. clathratum canopy (1-m2 portions) had no long-term effect on the abundance of A. clathratum,which within 14 months had recolonized most ofthe cleared areas. In contrast to juvenile A. clathra-tum, the abundance of P. serrata rapidly decreasedafter canopy removal. Our results demonstrate thatA. clathratum stands are a stable component ofurchin barrens in spite of the heavy grazing thattypically occurs there. Maintenance and expansionof A. clathratum stands and associated flora appearto depend on positive interactions with self-defend-ed adult A. clathratum.

Key index words: Agarum clathratum; Agarumcribrosum; Alaria esculenta; community stability;disturbances; grazing; kelp; mixed linear models;positive interactions; Ptilota serrata; recruitment;resilience; spatial and temporal scales

Herbivory and competition often reduce the re-cruitment and survival of marine algae, and both these

types of negative interactions are thought to playkey roles in structuring marine communities (Randall1961, Lubchenco and Gaines 1981, Harrold and Reed1985, Lewis 1986). Less attention has been paid to thepotential positive effects of grazing-resistant algae onother algal species that are vulnerable to grazing(e.g. by interfering with the foraging of herbivoresand providing microhabitats permitting increasedalgal recruitment and survival; but see Hay 1986, Pfis-ter and Hay 1988, Gagnon et al. 2003a) in spite of theincreasing recognition of the importance of positiveinteractions (i.e. facilitation) in structuring communi-ties (Bruno and Bertness 2001).

This bias is evident in polar and temperate regions,where herbivory (Dayton et al. 1984, Keats et al. 1990,Gagnon et al. 2004) and competition (Johnson andMann 1988, Paine 1990, Reed 1990, Leinaas andChristie 1996) can strongly affect the abundance anddistribution of macrophytes, although abiotic factorssuch as light availability, water motion, nutrients, sed-imentation, salinity, and ice scour are clearly importantas well (Dean and Jacobsen 1984, Dayton 1985, Ebe-ling et al. 1985, Keats et al. 1985). Intensive herbivoryhas been well documented in the subtidal zone in thenorthwestern North Atlantic where the green sea ur-chin, Strongylocentrotus droebachiensis, severely limits thedistribution of kelp beds (Himmelman 1969, Breenand Mann 1976, Chapman 1981, Scheibling et al.1999, Gagnon et al. 2004). Kelps are often restrictedto shallow water refuges but rapidly extend to deeperwater when urchins are naturally or experimentallyremoved (Himmelman et al. 1983, Scheibling 1986,Keats et al. 1990).

As elsewhere, the intensive grazing of S. droebachien-sis has led to the formation of extensive urchin barrensin the Mingan Islands (northern Gulf of St. Lawrence,Canada), which generally lack fleshy macrophytesand are instead dominated by calcareous red algae(Gagnon et al. 2004). Agarum clathratum and Desmarestiaviridis are the only two brown algae (Phaeophyta) reg-ularly found on these barrens. Agarum clathratum is aperennial kelp with a large holdfast, a rigid stipe, and alarge crinkled frond that becomes thicker and tougherwith age. Urchins have a low preference for this alga,possibly because of chemical deterrents (e.g. phenolics)(Vadas 1977, Larson et al. 1980, Himmelman andNedelec 1990). Although A. clathratum is most oftenfound in small stands (1–10 m2) on urchin barrens, itsometimes forms large stands (4500 m2) at the lower

1Received 30 January 2004. Accepted 1 February 2005.2Present address: Hyperspectral Data International, 7071 Bayers

Road - Suite 119, Halifax, Nova Scotia, Canada, B3L 2C2.E-mail: patrick.gagnon@hdi.ns.ca.

3Author for correspondence: e-mail Ladd.Johnson@b.o.ulaval.ca.

498

J. Phycol. 41, 498–505 (2005)r 2005 Phycological Society of AmericaDOI: 10.1111/j.1529-8817.2005.00078.x

edge of shallow beds of the kelp Alaria esculenta in ex-posed areas (personal observation). Elsewhere, A. cla-thratum has been shown to be competitively inferior toother kelp species and is thought to require some levelof grazing to suppress competitors (Vadas 1968). Incontrast, D. viridis is an annual species that appears tosurvive by rapid growth to a size at which its fine del-icate branching provides a mechanical defense againstgrazing (Gagnon et al. 2003a).

Although distinct invertebrate assemblages are as-sociated with stands of A. clathratum (Begin et al. 2004),nothing is known of the potential effects of A. clathra-tum on other algae in spite of its ability to reduce urchinabundance and restrict their movements (Gagnonet al. 2004). Moreover, we know little about the tem-poral or spatial stability of this conspicuous componentof the urchin barrens. In this study, we examine thetemporal variability in the distribution of A. clathratumand associated algae on urchin barrens in the MinganIslands. Specifically, we 1) examine temporal variabilityin the size of individual stands of A. clathratum; 2)quantify temporal changes in the abundance and dis-tribution of A. clathratum over large areas; 3) quantifythe distribution of juvenile A. clathratum, the red algaPtilota serrata, and urchins in the vicinity of stands ofA. clathratum; and 4) experimentally assess the impactof an A. clathratum canopy on the recruitment andabundance of algae.

MATERIALS AND METHODS

Study sites. Our study was conducted from 1998 to 2002(observations limited to the summer and fall) in the subtidalzone on the eastern side of Ile aux Goelands and on thewestern side of Petite Ile au Marteau in the Mingan Islands,northern Gulf of St. Lawrence (see Fig. 2 in Gagnon et al.2004). At each site, the bottom was a gently sloped bedrockplatform covered by a dense kelp bed, primarily Alaria escu-lenta, to a depth of 3–5 m. Below this shallow kelp bed, anurchin barrens extended a considerable distance (approxi-mately 200 m from the shore at Ile aux Goelands and 150 mat Petite Ile au Marteau) to a depth of approximately 10 m,where vertical walls began. The only fleshy macrophytescommonly found on the barrens at the two sites were thebrown algae Agarum clathratum and D. viridis, although smallpatches of the red alga P. serrata were also present, especiallyat greater depths.

Temporal variability in abundance and distribution of Agarumclathratum. To evaluate the variability in the abundance anddistribution of A. clathratum, we monitored changes in one12 � 12-m (144 m2) area in the barrens at each site. Thesesites were selected after exploratory surveys based on thesimilarity in stand configuration, that is, distinct stands ofA. clathratum separated by large areas without fleshy algae.Although the abundance of A. clathratum was somewhat high-er at these sites than on most urchin barrens in this region,these sites were selected because the clear boundaries of thestands increased our ability to detect changes in the abun-dance and distribution of A. clathratum and because the proxi-mity of the sites to our laboratory facilitated sampling.

At each site, we permanently marked the corners of thesampling area with bolts set into the bedrock. We subdividedeach area into an 8 � 8 sampling grid of 64 contiguous1.5 � 1.5-m plots using the following procedure. We first de-lineated two facing sides of the area with 12-m benchmark lines

tied to bolts and marked at 1.5-m intervals. A 1.5 � 12-m sec-tion was then defined by attaching two 12-m transect lines tothe benchmark lines and then subdivided into eight plots usinga 1.5 � 1.5-m quadrat positioned using the marks at 1.5-m in-tervals on the transect lines. Transect lines were then shifted tothe adjacent 1.5 � 12-m section and the sampling repeateduntil the entire area was sampled. Within each plot, the samediver estimated the percent cover of A. clathratum at five timesover a 2-year period (June 2000, August 2000, June 2001,August 2001, and June 2002). Benchmarks and transect lineswere removed between sampling periods.

Temporal variability in the size of Agarum clathratum stands.To evaluate changes in the size of stands of A. clathratum overtime, we monitored the surface area of 12 haphazardly se-lected stands of adult A. clathratum near the permanent12 � 12-m area at the Ile aux Goelands site. For each stand,we marked its position with a bolt set into the substratum atthe edge of the stand and then recorded to the nearest 1 cm1) the longest distance across the stand (A) and 2) the longestdistance running perpendicular to the first axis (B). Giventhat most of the stands were ellipsoidal in shape (even whenadjacent stands merges [see below]), we approximated thesurface area (S) of each stand using the equation S 5 p (A/2)(B/2). Sampling was done five times over a 2-year period(July 1999, May 2000, August 2000, June 2001, and July2001). Initial surface area of the stands ranged from 1.6to 12.8 m2.

Distribution of algae and urchins near Agarum clathra-tum. To determine whether stands of adult A. clathratumare associated with fewer urchins and increased algal recruit-ment, we compared the abundance of juvenile A. clathratum(i.e. o10 cm long), P. serrata, and urchins at the center of thestand with that at different distances from the edge of stands.Six haphazardly chosen A. clathratum stands (average width of2.4 m, SD 5 0.6, and stands separated by 44 m) were sam-pled on the eastern side of Ile aux Goelands in July 2000. Foreach stand, we counted the numbers of juvenile A. clathratumand urchins and estimated the percent cover of P. serrata in25 � 25-cm quadrats placed east and west of the centralpoint of the stand and also at 0, 50, and 100 cm from theeastern and western edges of the stand for a total of eightquadrats per stand, two for each of four locations (only themean of the east and west quadrats for each location was usedin the analysis). Unlike the other two common brown algae atthis site (D. viridis and Alaria esculenta), which can sweep backand forth across the substratum (Gagnon et al. 2003a,b),A. clathratum has an upright and rigid stipe that limits thesweeping action of the alga. Thus, the impact of the sweepingfronds of the individuals at the periphery of the stands de-creased rapidly, moving away from the edge and was virtuallynull at a distance of 100 cm, even under wavy conditions.Thus, our sampling covered the full possible gradient of theimpact of A. clathratum at the edge of the stands.

Effect of Agarum clathratum canopy on recruitment and abun-dance of algae. To assess experimentally the impact ofA. clathratum on the recruitment and abundance of algae onurchin barrens, we monitored changes in the density of ju-venile A. clathratum and percent cover of P. serrata in the ab-sence and presence of a canopy of adult A. clathratum over 14months. The two treatments consisted of 1-m2 areas in whichA. clathratum was experimentally removed and controls inwhich A. clathratum was left intact. Individuals were removedby cutting through the holdfast as close to the substratum aspossible. We also removed the distal portions of the blades ofA. clathratum surrounding the cleared areas to eliminate pos-sible impacts of algal sweeping on subsequent recruitment ofalgae. For this experiment, we used two large (450 m2) ob-long stands of A. clathratum that ran parallel to the shore at3–4 m in depth at Ile aux Goelands. In August 1998 we

KELP PATCH DYNAMICS IN URCHIN BARRENS 499

selected 16 1-m2 plots, spaced at 1–2 m intervals along thelower edges of the stands, and marked each with a bolt in thecenter. The plots were grouped into eight blocks of two ad-jacent 1-m2 areas, and one of the two was randomly chosenfor canopy removal. Stands were then sampled five times:August 1998 (1 day after canopy removal), October 1998,June 1999, August 1999, and October 1999. Each time, weestimated the number of juvenile A. clathratum and the per-cent cover of P. serrata in each plot using two quadrats(25 � 25 cm) placed on the north and south sides of the cen-ter bolt. After a heavy recruitment of the kelps A. clathratumand A. esculenta during the winter of 1998–1999, we were notable to separate juveniles and adults in 1999 due to logisticconstraints. We averaged the data from the two quadrats ineach area before comparing species abundance betweentreatments.

Statistical analysis. We used a repeated-measures (split-plot) analysis of variance (ANOVA) (Hand and Taylor 1987,Crowder and Hand 1990) to examine temporal changes inthe percent cover of A. clathratum in the 8 � 8 observationplots on the barrens with the factors Site (Ile aux Goelandsand Petite Ile au Marteau) and Time (five sampling dates)and with one nested element (Plots within Site). To take intoaccount the spatial dependency among the 64 plots at eachsite, we modeled the covariance structure with an exponen-tial correlation structure (Proc Mixed, type 5 SP(exp)(longi-tude latitude), SAS Institute Inc. 1999) (see Gagnon et al.2003a,b for other examples of the use of mixed linear mod-els). In this model, the correlation between the plots de-creased exponentially with the distance separating them,which provided the best fit of the model relative to othercorrelation structures, as judged by the value of the AIC cri-terion (Proc Mixed, SAS Institute Inc. 1999). The use of thiscorrelation structure has an effect equivalent to a reductionin the degrees of freedom, although this effect is not appar-ent in the ANOVA table (i.e. the degrees of freedom shownare equivalent to that of a model without a spatial correlationstructure). The temporal dependency was modeled with afirst-order autoregressive structure (Proc Mixed, type 5 SP(pow)(month), SAS Institute Inc. 1999) common to bothsites. Because no transformation corrected the lack of norma-lity in the data on some observation dates, the ANOVA wasalso run with the rank transformed data. Because both anal-yses gave similar results, we presented the results from theanalysis of the raw data as suggested by Conover (1980).

We analyzed temporal changes in the size of stands ofA. clathratum using a repeated-measures ANOVA with the fac-tor Time (five sampling periods). By June 2001, four pairs ofthe 12 original stands had merged together and the 4 otherstands had merged with stands that we were not monitoring (allremained merged until the end of our study). For each of thefour merging pairs of original stands, the surface area of thesmallest stand at the beginning of the study was given a value ofnull (0) in the analysis in June and July 2001 and the surfacearea of the merging stands was attributed to the other (largest)stand. This procedure introduced additional variability in thedata but minimized artificial increases in the size of the stands.Because variances fluctuated over time, we modeled the covar-iance structure with a specific heterogeneous compound sym-metry structure (Proc Mixed, type 5 CSH, SAS Institute Inc.1999). We applied the analysis to the raw data as the data foreach sampling date were normally distributed.

To evaluate the effect of A. clathratum on the abundance ofjuvenile A. clathratum, P. serrata, and urchins, we applied one-way ANOVAs (Zar 1999) with the factor Location (center of thestand, 0, 50, and 100 cm from the edge of the stand). The rawdata were analyzed for urchin density, whereas numbers ofjuvenile A. clathratum were square-root transformed to correctfor heteroscedasticity. Because no transformations corrected

for the heteroscedasticity detected in the raw data on the per-cent cover of P. serrata, the ANOVA was also applied to the ranktransformed data. Because both analyses gave similar results,we presented the raw data (Conover 1980).

To examine temporal changes in the density of A. clathratumjuveniles and P. serrata in the absence and presence of a canopyof A. clathratum, we conducted a repeated measures (split-split-plot) ANOVA for each species with the primary factor Stand(two stands of A. clathratum) and secondary factors Treatment(with/without canopy) and Time (August and October 1998and June, August, and October 1999). The final factor, Block,was treated as a random factor nested within Stand. Becausevariances were stable over time within the stands and the cor-relation in the data over time was similar between the treat-ments, we used a pooled covariance structure in the ANOVA(Proc Mixed, type 5 CS, SAS Institute Inc. 1999). We appliedthe analysis to the raw numbers on A. clathratum as the data foreach time were normally distributed, whereas the data for thepercent cover of P. serrata were square-root transformed toobtain normality for each observation date.

In the above analyses, normality was verified using Shapiro-Wilk’s statistic (SAS Institute Inc. 1999) and homoscedasticityby examining the graphical distribution of the residuals and byapplying the Levene test (Snedecor and Cochran 1989). Todetect differences among levels within a factor, we used least-square means multiple comparisons tests (LS means, SAS In-stitute Inc. 1999). A significance level of 0.05 was used for allstatistical tests.

RESULTS

Temporal variability in abundance and distribution ofAgarum clathratum. The 2-year monitoring of the12 � 12-m observation areas on the barrens indicat-ed that small, but significant, increases in the abun-dance of A. clathratum occurred at both sites betweenthe first (June 2000) and the last (June 2002) sam-pling dates (Table 1, Fig. 1), although site-specificfluctuations also occurred during this period. At Ileaux Goelands, the abundance of A. clathratum de-creased slightly during the first 2 months but in-creased steadily (approximately 0.7% �month� 1)after August 2000 and was 11.4% greater at the endthan at the beginning of the study (LS means,Po0.0001). At Petite Ile au Marteau, more substan-tial increases and decreases occurred during thestudy, including an approximately 25% increase

TABLE 1. Summary of the repeated-measures (split-plot)ANOVA (mixed linear model with spatial and temporalcorrelation structure; see text for details) showing the effectof Site (Ile aux Goelands and Petite Ile au Marteau) andTime (June 2000, August 2000, June 2001, August 2001,and June 2002) on the percent cover of Agarum clathratumin 12 � 12-m areas of urchin barrens (as averaged from 64plots of 1.5 � 1.5 m at each site).

Source of variation df F value P

Site 1 0.33 0.56Plots (Site) 126Time 4 42.26 o0.0001Site � Time 4 12.37 o0.0001Errora 504Total 639

aError 5 Time � Plots (Site).

PATRICK GAGNON ET AL.500

between August 2000 and June 2001, but the percentcover of A. clathratum at the end of the study was only6.5% greater than at the beginning.

The distribution of A. clathratum appeared to bestable at both sites (Fig. 2). At Ile aux Goelands, thegeneral gradual increase in A. clathratum was due tocolonization along the edges of stands, which werearound one large area of barrens (Fig. 2, upper rightcorner). Agarum clathratum was more patchily distri-buted at Petite Ile au Marteau and the observed fluc-tuations in abundance occurred across the grid.

Temporal variability in the size of Agarum clathratumstands. During the first year of the 2-year monitoringof the size of stands of A. clathratum, there was nosignificant change in area (Fig. 3; LS means,P 5 0.22). In contrast, stand area increased greatly(a 95% increase, corresponding to 11% �month� 1)between August 2000 and June 2001 (LS means,P 5 0.048) due primarily to the merging of standsafter incremental increases at the margins of stands(all the stands merged with other stands; four withstands we were monitoring and four others withstands that we were not monitoring). The 17%increase in size of stands observed in the last monthof the study (June 2001 to July 2001) was not signi-ficant (LS means, P 5 0.51).

Distribution of algae and urchins near Agarum cla-thratum. An inverse pattern of abundance of algaeand urchins occurred inside and around stands ofadult A. clathratum (Fig. 4). The density of juvenile A.clathratum and percent cover of P. serrata were ordersof magnitude greater inside than outside the stands,whereas the density of urchins inside was only a fifthof that outside the stands. No differences in the abun-dance of urchins and algae were seen at differentdistances from the edge of the stands (sampling at 0,50, and 100 cm, Fig. 4), consistent with the idea thatthe effect of A. clathratum on urchins and algae is lim-ited to the area within stands. The overall proportion

of small (o2 cm in test diameter) urchins (53.9%) wasgreater than that of medium (2–4 cm test diameter)(33.5%) and large (44 cm test diameter) urchins(12.6%) combined. Inside the stands, only 2.5% ofthe urchins were large, the large urchins were morenumerous outside the stands (13.3%, 13.9%, and11.9% of the individuals at 0, 50, and 100 cm fromthe edge of the stands, respectively).

Effect of Agarum clathratum canopy on recruitmentand abundance of algae. The 14-month monitoring of

FIG. 1. Changes over 2 years in the mean percent cover(� SE) of kelp Agarum clathratum on urchin barrens at Ile auxGoelands and Petite Ile au Marteau. Values not sharing the sameletter (small letters for Petite Ile au Marteau, capitals for Ile auxGoelands) are different (LS means, Po0.05). Asterisks indicatedifferences between islands in the change in percent cover (i.e.the slopes) during four successive sampling periods (group con-trasts, *Po0.05, **Po0.01, ***Po0.001).

FIG. 2. Changes over 2 years in the distribution and abun-dance of kelp Agarum clathratum in a 12 � 12-m zone of urchinbarrens at Ile aux Goelands and Petite Ile au Marteau. Dashedlines represent the position of transect lines used to divide eachzone into a sampling grid of 64 contiguous 1.5 � 1.5-m plots.

KELP PATCH DYNAMICS IN URCHIN BARRENS 501

changes in the numbers of juvenile A. clathratum andpercent cover of P. serrata in the absence and presenceof a canopy of A. clathratum indicated that the canopyhad little or no effect on the recruitment ofA. clathratum but had a large effect on the abundanceof P. serrata (Table 2, Fig. 5). The density of juvenileA. clathratum did not differ between treatments ex-cept in June 1999 when densities were almost doublein the presence of a canopy (4250 �m�2). Unfortu-nately, because we did not distinguish between adultsand juveniles during this and subsequent samplings,part of this difference was due to the inclusion of theadult algae that formed the canopy itself. However,given that densities of adults are typically near50 �m� 2 and the generally high recruitment of bothA. clathratum and the kelp Alaria esculenta (see below)that occurred between October 1998 and June 1999,we attribute this difference primarily to higher re-cruitment in treatments with an adult canopy. Re-gardless, this difference did not persist and the twotreatments were statistically indistinguishable by theend of the season.

In contrast, differences in the abundance of P. serratawere apparent from the beginning and persisted untilthe end. One day after the removal of the canopy, themean percent cover of P. serrata fell to o50% of thatseen in areas with an A. clathratum canopy, althoughthis difference was not significant (LS means,P 5 0.10). In the treatment with a canopy, the coverof P. serrata generally increased during the study andby October 1999 was 53% greater than at the begin-ning of the study (Fig. 5). Although there was not astatistical difference between the first and last date ofthe study, the cover was significantly greater on thepenultimate sampling date (LS means, P 5 0.0054). Incontrast, in the areas with the canopy removed thecover of P. serrata remained low (o5.3%) throughoutthe study and was only 17% of that in control areas bythe end of the study (LS means, P 5 0.0003; Fig. 5).

In areas with and without a canopy, the percentcover of other noncalcareous algae (e.g. ulvoid algae,

diatoms, and the red algae Phycodrys rubens and Por-phyra sp.) was always low (o5%). The exception was asubstantial recruitment of A. esculenta between October1998 and June 1999 that appeared to be greater in thepresence (93.0 �m� 2, SD 5 69.4) than in the absence(65.1 �m� 2, SD 5 24.2) of an A. clathratum canopy. This

FIG. 3. Changes over 2 years in the mean surface area (þSE)of stands of adult kelp Agarum clathratum (n 5 12 for each sam-pling date). The arrow indicates the time at which we first ob-served mergers between the stands. Values not sharing the sameletter are different (LS means, Po0.05).

FIG. 4. Mean density and percent cover (þ SE) of the greensea urchin Strongylocentrotus droebachiensis, juvenile kelp Agarumclathratum, and the red alga Ptilota serrata at different distancesfrom the center of stands of adult A. clathratum. For juvenileA. clathratum, the data have been back-transformed from thetransformed data used in the analysis. Values not sharing thesame letter are different (LS means, Po0.05).

PATRICK GAGNON ET AL.502

difference was not significant (LS means, P 5 0.39), butAlaria esculenta recruits completely disappeared fromareas with a canopy by August 1999, whereas theywere still common in treatments where the canopy wasremoved (38.0 �m�2, SD 5 18.3). At the end of thestudy (October 1999), A. esculenta was absent in bothtreatments.

DISCUSSION

Agarum clathratum stands are a persistent (sensuDayton et al. 1984) feature of urchin barrens. In our12 � 12-m observation areas, this species maintained acover of 445% over a 2-year period and was even ableto increase in abundance in spite of the intensive graz-ing by urchins (Gagnon et al. 2004). Increases weredue to the gradual enlargement of existing standsrather than to the formation of new stands, withexpansion or recession occurring along the edge ofstands and no change in the central areas. Our obser-vations of individual stands were consistent with theselarger scale trends as the stands increased both mar-ginally and by merging.

Much of our knowledge about the ecology ofA. clathratum comes from the pioneering work of Vadas(1968) in the northeastern North Pacific. He foundthat 1) the growth of A. clathratum is greatest duringlate fall, winter, and early spring (when water temper-atures are at their lowest); 2) A. clathratum can becomeestablished during the fall and winter seasons, whenthe majority of potential competitors (other kelp spe-

cies) are unable to develop; and 3) A. clathratum iscompetitively inferior to other kelp species and canonly become established when urchins (Strongylo-centrotus droebachiensis and Strongylocentrotus francisc-anus) are present. Results of our experimental remov-al of the A. clathratum canopy were generally consistentwith these observations, for example, the greatest re-cruitment of A. clathratum occurred between the midfall and the late spring. The pattern of the recovery ofstands of A. clathratum was also consistent with the ideathat grazers are required to suppress other species, butother factors may have also contributed. In particular,when A. esculenta recruits were first observed (June1999), their density was less than half that of A.clathratum, suggesting that A. clathratum had a numer-ic advantage if competition among juvenile stages wasimportant. The rapid decline of A. esculenta in thepresence of an adult A. clathratum gives further supportto the importance of competition in its establishment.Still, selective herbivory by the green sea urchin wasprobably involved as urchins consume A. clathratum ata much lower rate than species of Alaria (Vadas 1977,Larson et al. 1980, Himmelman 1984, Himmelmanand Nedelec 1990), and A. clathratum has been ob-served to replace Alaria esculenta at the edge of anA. esculenta bed where urchins were most abundant

TABLE 2. Summary of the repeated-measures (split-split-plot) ANOVA (mixed linear model) showing the effect ofStand (two stands), Treatment (with or without a canopy ofAgarum clathratum), and Time (August 1998, October 1998,June 1999, August 1999, and October 1999) on the meandensity of A. clathratum and percent cover of Ptilota serrata inthe A. clathratum canopy-removal experiment.

Source of variation df

Agarum clathratum Ptilota serrata

F value P F value P

Main plotStand 1 0.97 0.36 2.61 0.16Block (Stand)a 6 — — — —

Sub-plotTreatment 1 4.88 0.069 13.85 0.0098Treatment � Stand 1 0.89 0.38 0.17 0.70Treatment � Block

(Stand)b6 — — — —

Sub-sub-plotTime 4 23.12 o0.0001 2.08 0.0990Time � Stand 4 5.24 0.0014 1.60 0.19Time � Treatment 4 1.84 0.14 4.18 0.0056Time � Stand �

Treatment4 0.14 0.97 0.10 0.98

Errorc 47Total 78

Data on P. serrata were square-root transformed.aMain plot error.bSub-plot error.cError 5 Time � Block (Stand)þTime � Treatment � Block

(Stand) 5 Sub-sub-plot error.

FIG. 5. Changes over 14 months in the mean density (þ SE)of kelp Agarum clathratum and percent cover of the red algaPtilota serrata in the absence and presence of a canopy ofA. clathratum. The arrow indicates the time from which the sam-pling was conducted without discrimination between juvenileand adult stages of A. clathratum. Values not sharing the sameletter (small letters for A. clathratum, capitals for P. serrata) aredifferent (LS means, Po0.05).

KELP PATCH DYNAMICS IN URCHIN BARRENS 503

(Gagnon et al. 2004). Regardless, our observations in-dicate that A. clathratum is resilient to punctual small-scale (approximately 1 m) disturbances, which shouldpermit A. clathratum to recover from disturbances bystorms and ice scour, which often occur in Newfound-land and the Gulf of St. Lawrence (Hooper 1981,Keats et al. 1985, Gagnon et al. 2004).

The spatial and temporal stability of A. clathratumstands should favor associations with algae or algalstages that are more vulnerable to grazing or to dis-lodgment by currents and waves. Our observation thatA. clathratum juveniles and the red alga P. serrata weremore abundant within the stands of adult A. clathratum,where urchin densities were reduced, suggests thatA. clathratum stands provide certain understory algalspecies with protection from urchin grazing. However,our experiments only partially support this idea.Recruitment and recovery of A. clathratum in small dis-turbed areas did not require the presence of an adultcanopy, although it appears that densities of bothA. clathratum and Alaria esculenta recruits were higherin the presence of the canopy during the initial phasesof colonization (i.e. during the winter–spring period).Alternatively, the association of recruitment of A.clathratum with adult stands could be linked to a high-er density of gametophytes under the canopy. The re-moval of the canopy would then not have had animmediate effect on recruitment because there mayhave been a bank of gametophytes already presentwhen the experiment was initiated.

In contrast, there was a clear positive effect ofA. clathratum on P. serrata as removal of the canopylead to a rapid and persistent decrease in its abun-dance. More detailed investigations are needed to de-termine the exact mechanism by which A. clathratumenhances the recruitment of P. serrata. Reduced graz-ing is a possibility (S. droebachiensis has a very low at-traction to and feeding rate on P. serrata in the MinganIslands; Himmelman and Nedelec 1990), and previousstudies have shown that mechanical abrasion fromwave-induced movement of algal fronds repulses ur-chins (Konar 2000, Gagnon et al. 2003a). Whether thestiff and upright fronds of A. clathratum provide thistype of protection remains to be determined. The den-sity of the rigid stipes of adult A. clathratum might alsolimit the movement of urchins into the beds (less spaceto move around). It is also possible that P. serrata ismore abundant under A. clathratum because the cano-py protects it from being broken or dislodged by wavesand currents. Ptilota serrata is often weakly attached(personal observation), and macrophyte canopies havebeen shown to reduce flow (Eckman et al. 1989, Ack-erman and Okubo 1993). This mechanism could ex-plain the pronounced decrease in the abundance ofP. serrata immediately after the removal of the A.clathratum canopy. Alternatively, this decrease couldbe partially the result of the technique we used toremove A. clathratum, which may have disturbed neigh-boring clumps of P. serrata in spite of efforts to avoidsuch effects. Finally, the A. clathratum canopy might

enhance the recruitment of P. serrata by providing suit-able light conditions. Indeed, P. serrata appears to beshade tolerant, because in the Mingan Islands it is al-most exclusively found under kelp canopies or on barerock at greater depths (personal observation). If so,then the low number and small size of urchins underthe canopy were probably not sufficient to reduce theabundance of P. serrata, which could then outcompeteAlaria esculenta and reach a size invulnerable to grazingby urchins. The positive effects of stands of A. clathra-tum on the recruitment of algae on urchin barrens didnot extend to D. viridis, the other common brown algaof this habitat. This annual species is not associatedwith stands of A. clathratum. Rather, it appears to col-onize the barrens by recruiting in the winter, whenurchin grazing activity is low, and then relies partiallyon mechanical repulsion of urchins once it reaches alarger size (Gagnon 2003).

A critical question is how stands of A. clathratum areinitially formed. We previously showed that juvenileA. clathratum are avidly consumed by urchins whenother algal foods are not available but protected to adegree when associated with D. viridis (Gagnon et al.2003a). However, because D. viridis is an annual, thisprotection is short lived. We still do not know howjuvenile A. clathratum can survive for longer periodsoutside of stands of adults. Perhaps an exceptional yearof massive recruitment is required. Longer term andlarger scale studies are needed to answer this question.

Our study is the first to examine the temporalchanges in algal assemblages on urchin barrens inthe northwestern North Atlantic. We show that thespatial and temporal stability of stands of A. clathratumcan be high, in contrast to other kelps that are readilygrazed by the green sea urchin (Breen and Mann1976, Scheibling et al. 1999, Gagnon et al. 2004).This stability may be due, in part, to the enhanced re-cruitment of juveniles in adult stands of A. clathratum.These stands also increase diversity by increasing theabundance of P. serrata (this study) as well as associatedinvertebrates (Begin et al. 2004). As demonstrated forD. viridis (Gagnon et al. 2003a), this situation repre-sents a facilitative interaction (Connell and Slatyer1977, Callaway 1995, Bruno and Bertness 2001) thatpermits algal recruitment and survival on urchinbarrens. Further studies are needed to determinehow A. clathratum and D. viridis withstand urchin graz-ing during juvenile stages and to estimate the relativecontribution of adult A. clathratum and D. viridis inmaintaining algal assemblages in this intensivelygrazed environment.

We are grateful to N. Cormier, O. D’Amours, J.-F. Raymond,P. Gauthier, L.-P. Cote, T. Gosselin, S.-P. Gingras, M. Dionne,B. Laberge, V. Messier, and M. Thompson for their help dur-ing the intensive field seasons (including long dives incold water) and to G. Daigle for statistical advice. Thanksalso to two anonymous reviewers for thorough revisions ofearlier drafts of the manuscript. This research was supportedby NSERC (Natural Sciences and Engineering ResearchCouncil of Canada) and FCAR (Fonds pour la Formation

PATRICK GAGNON ET AL.504

de Chercheurs et l’Aide a la Recherche) grants (to J. H. H andL. E. J.). P. G. was supported by FCAR, NSERC, and Quebec-Ocean scholarships.

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