Marine Biology 84, 287-294 (1985) Marine

...... Biology Springer-Verlag 1985

Severe storm disturbances and reversal of community structure in a southern California forest

A. W. Ebeling, D. R. Laur and R. J. Rowley

Department of Biological Sciences and Marine Science Institute, University of California at Santa Barbara; Santa Barbara, California 93106, USA

Abstract amounts of primary substrate were cleared and settled by new growths of sessile organisms, and change in community Regular observations made over a period of 5 yr in four structure varied with degree of exposure to the full force of permanent transects provided data on plant, , the waves. Such changes will persist only if the disturbance and fish densities which indicate that two unusually severe rate exceeds recovery time. Hence, geographic differences winter storms in t980 ("Storm I") and 1983 ("Storm It") in storm frequency may account for observed differences had different effects on a southern California kelp-forest in the community structure (Goreau, 1959). However, in community. Storm I removed all canopies of the giant kelp places where severe storms are rare, such as Jamaica , but spared most understory , (Woodley etal., 1981) and southern California (Dayton mainly Pterygophora californica. Hence, the previously and Tegner, 1984), the community may either undergo large accumulation of detached drift kelp, mostly cycles of alteration and recovery (Connell and Sousa, M. pyrifera, disappeared. Denied their preferred diet of 1983) or persist in the altered state if recovery time is long drift kelp, the sea urchins Strongylocentrotusfranciscanus (Sutherland, 1981). and S.purpuratus then emerged from shelters to find Recovery time of subtidal kelp forests in temperate alternative food. Without effective predators, they con- waters may be delayed by grazing sea urchins if the sumed most living plants, including the surviving under- urchins have neither adequate detrital food nor effective story kelps. This weakened the important detritus-based predator control. In a mature forest, most of the annual food chain, as indicated indirectly by declining abundances production of kelps forms a litter of detached drift (Gerard, of algal turf and fish (Embiotocidae) that eat small 1976). Urchins readily eat such drift (Vadas, 1977) and animals living in turf. In 1983, Storm II reversed the usually spare living plants wherever sufficient supplies are process by eliminating exposed urchins, while clearing available (e.g. Lowry and Pearse, 1973; Rosenthal etal., rock surfaces for widespread kelp settlement and growth. 1974). If the forest is destroyed by severe storms or other By summer 1984, the kelp grew to maturity to form agencies, the urchins may have no drift to eat (see Harrold extensive canopies despite elevated water temperatures and Reed, 1984). If uncontrolled by predators, disease, or during summer and fall of 1983. Thus, severe storms may water motion, the urchins will then move out over the reef have vastly different effects on community structure, to graze back new growth and form a "barrens" covered depending on the state of the community before the with little more than crustose algae and patches of low turf disturbance. (Lawrence, 1975). Urchins are able to remain in a barrens because they can subsist on little food (Ebert, 1967; Lang and Mann, 1976). This prevents recovery of the important detritus-based food chain (see Mann, 1982), which gener- Introduction ates much of the small invertebrate prey that fish eat (Mann, 1977; Simenstad etal., 1978; Laur and Ebeling, The frequency, magnitude, and scale of major storm 1983). Frequency-dependent foraging by sea otters disturbances may determine the structure of many kinds (Enhydra lutris) effectively controls numbers of exposed, of natural communities, including those of marine reefs grazing urchins in dense kelp forests off the Aleutian (Goreau, 1959; Conneli, I978; Paine, I979). For exampIe, Islands (e.g. Estes eta[., 1978), Alaska (Duggins, 1980), Woodley etaL (1981) described hurricane-induced per- and central California (Lowry and Pearse, 1973; Reed and turbations of a Jamaican coral-reef community: large Foster, 1984). Yet kelp grows abundantly off southern 288 A. W. Ebeling et al.: Storm disturbances of a

California where otters are absent and Where exposed NM in Fig. 1 D. This included intervals before and after urchins occur abundantly in barrens patches (e.g. Leighton the large storms of 1980 ("Storm I") and 1983 ("Storm II"). et al., 1966; Pearse et al., 1970; North, 1971; Tegner, 1980). Two transect sites (NE, SE) were in an extensive stand of Under such circumstances, kelp forests may be less resilient understory kelp over the reef base. Substrate at the NE and occur more sporadically (North, 1971), site was originally a mosaic of sand, cobble, and partly Thus, mature kelp forests and their productive detrital encrusted rock, but was scoured by Storm I. Throughout food chains may persist off southern California only most of the study the more protected SE site remained because storms powerful enough to destroy them and covered with sand merging with cobble. The two other eliminate drift kelp are rare here (see Dayton and Tegner, transect sites (M, NM) were near the reef top at 7 to 8 m 1984). Once destroyed, however, forests without a resource depth, among crests and rills with high urchin-densities, of drift may be slow to recover unless sea urchins are rich algal turf, and intense foraging by surfperch. Site M controlled (North, 1971; Wilson etal., 1980). Yet a storm was in a rill; Site NM was located along the north slope of strong enough to remove kelp may also remove urchins or the reef. Permanent 60 m transects of polypropylene rope alter their behavior, especially exposed individuals in had been anchored and maintained at Sites NE and NM barren areas (Cowen et al., 1982; Harrold and Reed, 1984). for fish censusing and other studies (see Ebeling and Laur, Thus, the process may be reversible. 1984). A similar transect was constructed at Site SE for In our study, we show that two unusually severe monitoring a persistent stand of understory keIp. At storms, which surprisingly struck coastal southern Cali- Midreef Site M, steel pins marked ends of a 13 m transect fornia only three years apart, started reversible processes. for measuring macroinvertebrate densities along the gently The first storm initiated a process leading to deforestation sloping side of a rill. of our study reef: drift kelp was eliminated, hungry Since the study was opportunistic, we could not pre- urchins left shelter, regrowth was grazed back, secondary design all sampling, and had to extend new observations production probably fell, and fish abundance declined. from previous ones made for other studies. Hence, not all The second storm, of similar force, initiated the process of monitoring was quantitative and not all measurements reforestation: exposed urchins were decimated, kelp were made at each transect site. The state of the kelp forest regrew, drift again accumulated on the bottom, and the before and after Storms I and II was mapped from field detritus food chain was restored. We attribute much of this notes and measurements made during reefwide surveys reversal in community form to marked changes in the throughout the 5 yr interval (Fig. 1). We feel that this is behavior, distribution, and abundance of grazing sea adequate because many changes were widespread and urchins. dramatic: for example, from a thick, continuous kelp forest We documented this by monitoring four important to an exposed "barrens". At least once a season, we components of the detrital food chain accounting for much surveyed the reef and redefined limits of kelp stands and of the obvious community structure at our study site: (1) substrate type. We counted kelp- recruits in kelps, both giant kelp Macrocystis pyrifera which forms a 0.25 m 2 quadrats near our transect sites during times of surface canopy, and the understory kelps Pterygophora maximum settlement. Water temperature was measured californica and Larninariafarfowii which rise less than 1 m semi-weekly at the surface and t3m depth during off the bottom; (2) algal turf which houses many of the 1979-1981, but not during 1982, and irregularly during secondary producers such as small crustaceans, mollusks, 1983. and worms; (3) grazing sea urchins Strongylocentrotus ReguLar observations of plant cover and of sea urchin franciscanus and S. yurpuratus; and (4) epibenthic fishes in and fish densities were averaged per bimonthly interval. the surfperch family Embiotocidae which are the principal Percent understory kelp cover was estimated once every exploiters of small invertebrate prey living in the turf two months in thirty 0.75 m 2 quadrats placed randomly (Laur and Ebeling, 1983). Results of this monitoring and along the NE transect both before and after Storm I, and other work provide a unique view of a reef community as along the SE transects after Storm I only. Similarly, we forest, as barrens, and in transition between the two condi- estimated algal turf cover in 15 quadrats along the NM tions. transect before and after Storm I. Sea urchin densities were measured 1 to 7 times within bimonthly intervals before and after Storm I at Transect Site M and occasionally Materials and methods after Storm I at Site NE. Since abundances of the two urchin were strongly correlated (r= 0.85, n = 69, We monitored densities of these four groups of organisms P<0.001), we pooled densities for counts of total adults at Naples Reef, an isolated outcrop of shale located 1.6 km in a 13 X 1 m band delimited by a meter bar pushed along offshore about 23 km west of Santa Barbara, southern the side of a nylon line stretched between two pins. California (34~ 119~ The reef covers 2.2 ha, Surfperch densities were of total adult and subadult ranges in depth from 5 to 15 m, and consists of a series _~ individuals of the 5 principal species inhabiting the reef rills and ridges running parallel to the coast (Ebeling et al., (see Laur and Ebeling, 1983; Ebeling and Laur, 1984): 1980). Regular observations were made during a 5 yr span Ernbiotoca jacksoni, E. lateralis, Hyysurus caryi, Rhacochilus in four permanent transect sites marked NE, SE, M, and toxotes, and Damalichthys vacca. We counted fish 4 to 10 A. W. Ebeling et al.: Storm disturbances of a kelp forest 289

A /////////////A/.7.'/.'/.'/'/'J:/r D

}30M I l SE SUMMER, 1979 PRE STORM | SPRING, 1981 'BARRENS'

.:: ~":"~..::::~:: : :~:: ::: :~::: g::: ;::~::::::: :::::::::::::5:::

SPR,NPOST STORM , 1980 I .... ] SPRING, 1983 " POST STORM II

C

FALL, 1980 " SUMMER, 1984

Fig. 1. Naples Reef, southern California, showing distributions of mature giant kelp, Macrocystis pyrifera (coarse hatching), mature understory kelp - mostly Pterygophora californica (large dots), newly recruited plants (fine hatching or small dots), major sea-urchin fronts (asterisks), and continuous rocky substrate (stippled) before and after Storms I and II. (D) gives scale (30 m), depth contours (7, 11, 15 m) and transect sites (bars marked NE, SE, M, NM)

times within bimonthly intervals (about weekly) along a tions. Bags were weighed full and empty (to subtract the transect line at Site NM, tallying all individuals seen weight of the bag) when returned to the diving skiff. within ~ space estimated to be 3 m wide over the bottom and extending 1.5 m upward. The litter of drift algae ("drift") was sampled at Naples Results and comparable reefs inshore about 6 km away. Unlike Naples, the inshore reefs were forested during the entire Kelp forest and reef 5 yr study period. Collected under dense stands of giant kelp, the inshore samples included drift from accumula- Storms I and II initiated periods of kelp loss and resettle- tions like those we saw (but did not sample) at Naples ment at Naples Reef (Fig. 1). In summer 1979 before before Storm I. Samples were taken by SCUBA divers Storm I, a large surface canopy of giant kelp, Macrocystis stuffing as much algae as they could into net bags during pyrifera, covered the reef (Fig. 1 A). It extended inshore, 5 min swims out from midreef in random compass direc- supported by holdfasts anchored to smaller reefs or even 290 A.W. Ebeling et al.: Storm disturbances of a kelp forest sand bottom (see North, t971). Large fields of understory surrounding base supported a dense canopy of new kelp kelp, mainly Pterygophora caIifornica with widely scattered some 5 to 40 cm tall (Fig. 1 E). Individuals of individuals of Larninaria farlowii, covered much of the Pterygophora californica outnumbered those of Macrocystis eastward reef base. Smaller stands extended south- pyrifera by about 10:1. Enough plants survived the fol- westward or formed patches on top of the reef. Then, for lowing calm summer and winter to produce well-devel- two weeks in February 1980, Storm I generated waves that oped surface and understory canopies in spring-summer reached the extraordinary height of 6 m in the Santa 1983, the first in the area since 1979 (Fig. 1 F). Kelp stands Barbara Channel (wave height data estimated front ARCO were destroyed only in the few places where adult red Oil Platform "Holly" and provided by C. Fusaro). This urchins were still abundant and could assemble as fronts was more than twice the maximum wave height recorded near new surfaces, At Site NM (Fig. 1 E, F), for example, during the previous 7yr (Harger, 1979). The powerful urchins had consumed all sporophytes by mid-August surge swept away sand, scoured off crusts of coralline 1983. Surviving the storm in deep refuges, these urchins algae, and broke off slabs of shale to create large areas of soon formed fronts and moved upslope to graze back all bare rock ("new surfaces"). Water motion removed all stands of young kelp and most algal turf before fall. canopies of giant kelp from Naples Reef and environs. Water temperature varied yearly as well as seasonally Most holdfasts from which stipes had been torn eventually (Fig. 2). Relative to typical seasonal values measured died. The nearest surviving kelp forest Was more than 6 km during 1979-1981, both surface and 13 m temperatures away. Yet the sturdier stipes of P. californica endured decreased as usual during the spring upwelling period of about the reef base to grow new blades during spring 1983, but then reached unusual highs during summer and 1980. This produced a new understory canopy unshaded fall 1983. by surface kelp. Kelp sporophytes recruited mostly to new surfaces in densities of about 50 m -~ (n=22). However, adult sea urchins soon left refuges in cracks and crevices to Algal drift graze back the new growth. Continued grazing by sea urchins eliminated most of Loss of giant kelp eliminated the main source of algal drift the remaining stands of macroalgae. This process was well (Table 1). Before Storm I, benthic accumulations on underway by fall 1980 (Fig. 1C). By then urchins had stripped the reef of new kelp sporophytes and most vegetative regrowth, primarily ofunderstory kelps anchored Table 1. Mean weights (+ SEM) of detached drift algae at Naples to continuous rock surfaces. The only surviving field of Reef and similar rocky inshore reefs. Means with different letters (in parentheses) are significantly different by analysis of variance understory kelp was at Site SE. Here, the sandy substrate of data values (x) transformed to log (x + 1) and Duncan's mul- seemed to deter a long front of large red sea urchins tiple-range test (P < 0.05). Storm I occurred in February 1980, (Strongylocentrotus franciscanus) advancing from the Storm II in February 1983 north. However, even the SE kelp stand was eliminated in spring 1981 (Fig. 1D). A gathering front of red urchins Locality and Date Depth n Mean wet wt date (m) (g) suddenly invaded the previously inviolate area of sandy substrate to destroy the whole stand (about 1 ha) within a InshoreReefl July-Aug. 1980 8-12 12 3 192+432(A) month (24 March-25 April). The community remained in Inshore Reef2 July-Aug. 1980 3-10 12 3 227_+606 (A) this barren condition until spring 1983. Naples Reef Following benign seasons of 1981 and 1982, the winter July-Aug. 1980 7-15 14 90_+ 27 (C) storm series of 1983 (Stoma II) was also unprecedented in Sep.-Oct. 1983 7 15 12 482_+111 (B) July- Aug. 1984 7 15 13 1 969-+ 184 (A) magnitude (see Dayton and Tegner, 1984). Waves again Inshore Reef 1 July-Aug. 1984 8-12 12 2 300-+ 159 (A) reached 6 m or more in height. The powerful surge created extensive new surfaces on Naples Reef, the first since 1980. (Measured during a 50min dive, 31 scars from 22 x Surface [1983 detached shale slabs averaged 1.3 m_+ 1.0 (SD) in breadth, • o13m about the same as scars produced by Storm I. Sand and 2O -- x~.-'\ • x rock scoured even larger areas.) Populations of exposed ? " o ", ",.--~-. Surface urchins on the elevated parts of the reef were decimated. v18 /. o x/ o x o\\ o "~ means, Only those individuals sheltering in deeper water about 16 the reef base were spared in substantial numbers. Kelp X c'< L-""(t~'-..~ it'/'~ / ~ x ll~m E 14 _--- ~ ~• / ~ ; means, sporophytes recruited to most reef areas (Fig. 1 E), but in ~ 1979 81 densities more than 10 times greater on new surfaces than 12

on old (Harris etal., 1984). Sporophytes averaged 558 m -2 10 on new surfaces at Transect Site M (Harris et aL, 1984) and I j I F I M I-A I M I j I j I A I S I O I N I D-I 518--+600 (SD) on similar surfaces at Site NM (n=28, Fig. 2. 1983 temperature readings from Naples Reef plotted on 0.25 m 2 quadrats placed haphazardly on new surfaces in envelopes delimiting the ranges of monthly means based on semi- June 1983). Thus, in spring 1983, most of the reef and weekly observations taken during 1979-1981 A. W. Ebeling et aL. Storm disturbances of a kelp forest 291

- 2 . Storm I 2 1.}_._ 4 Storm ][ :.. 60 300 -oo3 ~f9 "~ 40 200 ~ = 6 / a X "i" 4 2[ A ~ k .... Sea urchins at site M ~. / =S c-6 {.Jl__;_ I .'~. "~:" / XT~ ~ Kelp cover at NE(n=30) \ / O~ ::3" .~- " ~ "\ ~- -~ Kelp cover at SE \ 20 100 ~-~ I 't~_ L % 3" 0 0

20 . •--o Surfperch ] - NM -n20 9 ~10 e_ o Algal turf cover (n = 15) i a, / ~ ~81o_ 3,0 g_-

0 JIMIMIJ ISINIJ IMIMI JIsIN]jIMIMI J ISIN] {~ IMIjIsIN] jIMIMI J iSI 0 F A J A O OIV A J A 0 DIF A a A O D I J A O DIE A J A O 1979 1980 1981 1982 1983 Fig. 3. Strongylocentrotus franciscanus plus S. purpuratus, Pterygophora californica, Embiotocidae, and algal turf. Bimonthly means (+_ SEM) of pooled sea urchin counts (S. franciseanus+ S. purpuratus), percent cover of understory kelp (mostly P. californica), embiotocid surfperch densities, and percent cover of algal turf at monitored transect sites on Naples Reef (see Fig. 1 D) before and after Storms I and II. Numbers next to urchin and fish means are sample sizes

Naples Reef resembled those under inshore forests. tke start of the barrens period to over 23 rn -~ in I98t, as Detached Macrocystis pyrifera made up the greatest the ratio of species densities remained 3:1. Since thorough portion by far, followed by understory kelps and other searches revealed far fewer sheltering urchins, the increase , and small amounts of foliose red algae. After probably reflected an emergence of individuals that had Storm I, algal drift dropped to less than 100 g per sample been hiding before (see Russo, 1979; Harrold and Reed, and contained little or no kelp, as compared to more than 1984). Then after a series of smaller storms during fall- 3 kg of mostly M. pyrifera collected under a persistent winter 1982-1983, densities fell to nil with Storm lI in forest at an inshore reef about 6 km away. Drift algal 1983. During 1983-1984 the few adult immigrants sought abundance at Naples remained low throughout the shelter under boulders at the rill bottom. barrens period (July 1980 to March 1983), As noted Disruptions in normal seasonal cycles of understory above, kelp recruitment was high at Naples following kelp cover were related to increased densities of exposed Storm II, and the young forest began producing substantial sea urchins (Fig. 3: top graph). Although understory cover amounts of drift by falI t983. Reflecting forest structure, was measured at a different transect site (NE) than urchin this new supply included noticeable amounts of an early- densities (M), the relation was generally robust and held arriving, fast-growing species of non-iaminarian brown reefwide. Before Storm I at Site NE, the understory alga, Desmarestia spp., as well as abundant kelp. In and canopy had undergone its usual seasonal cycle of thinning about refuges, sea urchins held various bits and pieces from more than 50% cover in summer to about 15% cover of algae (80% of I00 pieces examined were held by one in winter (Fig. 3: top graph). We saw few urchins at Site or more urchins). By August 1984, drift again reached NE then, and no plants had been grazed. The abrupt amounts typical of summer accumulations under a ma- decline in cover in spring and summer 1980 occurred as ture kelp forest (Table I). large red urchins appeared, formed fronts, and consumed the plants. Storm II reduced urchin densities at Site NE from 3.2+0.5 (SEM) m -2 (n=5 haphazardly placed Sea urchin density and understory kelp cover transects) to 0.3_+0.1 (n=4), after which keIp recruited abundantly to the area (Fig. 1 E). By comparison, large red Sea urchin densities varied with conditions imposed by the urchins counted separately at Site M were reduced from two storms (Fig. 3: top graph). Before Storm I, densities of 5.6-+0.5m -2 (n=20 counts from September 1980 to exposed (countable) urchins of both species at Transect Storm II) to 0.4 _+ 0.1 (n = 23). Site M averaged 7.9 to 14.2m -2, with purple urchins Continued understory cover at Transect Site SE in- (Strongylocentrotus purpuratus) outnumbering red urchins dicated that, without urchin grazing, conditions favored (S.franeiscanus) by 3:1. The transect was on the sloping kelp growth after Storm I (Fig. 3: top graph). Ungrazed side of a rill, however, and we could see (but did not during 1980, understory kelp at Site SE underwent a full count) clusters of individuals sheltering in crevices and seasonal cycle of thinning and regrowth of blades after under boulders above and below the slope. After Storm I, Storm I. Urchins eventually invaded the sandy site and densities of exposed urchins doubled from March 1980 at eliminated plants in spring 1981. There was no subsequent 292 A.W. Ebeling et aI.: Storm disturbances of a kelp forest kelp recruitment to this area, which retained its sand cover either species could have prevented plant recolonization throughout the study. here because purple urchins outnumbered red urchins by 3:1. Even at the deeper and flatter site along the reef base (Fig. 1, Site NE), understory kelp cover was completely Surfperch density and turf cover destroyed where the ratio was only 0.5 : 1 and red urchins were fewer (2=3.2m -2) than at the midreef (5.6) before Embiotocid surfperch densities correlated strongly with Storm II. Furthermore, the grazing power of red urchins turf cover at Transect Site NM (Fig. 3: bottom graph; may be underestimated if it is based only on densities of r=0.80, P<0.001, n=21). Before StormI, both varied dispersed or stationary individuals. Such individuals may seasonally, increasing during the spring and summer. Both become more destructive when they aggregate as dense, fell during the barrens period between Storms I and II, moving fronts (Dean et aL, 1984). then increased after Storm II, though not to previous A comparison of kelp cover trends indicates that maxima. The site no longer attracted the abundance of seasonal regrowth after Storm I would have been normal surfperch recorded before Storm I. The abrupt decline in but for urchin grazing. Having durable holdfasts and turf cover after June 1983 occurred as fronts of urchins stipes (Reed and Foster, 1984), understory kelp plants grazed their way up the slope at this site (Fig. 1 E, F). grew new blades after Storm I, but were devoured by red Before this, however, cover of turf and of understory kelp urchins at Site NE during May-August 1980. Yet the appeared controlled by the same reefwide processes. process was delayed for almost a year in adjacent Site SE whose sandy substrate may have temporarily discouraged urchin movements (see Breen and Mann, 1976; Tegner Discussion and conclusions and Dayton, 1977). Dispersed over the whole reef, moving and grazing The two large storms marked periods of disappearance adult sea urchins may have prevented any large-scale and reappearance of a kelp forest. However, this reversal recruitment of kelp and other algae between storms. of community form was related less to the frequency of Urchins ate most living plants because the accumulation storm disturbance than to the magnitude and scale of of drift kelp and other algae was nil. They survived in the initial effects coupled with the frequency of biological open because they could subsist on alternative foods and disturbance by grazing sea urchins. The storms affected had few predators (see "Introduction"). In the absence of one part of the community directly and another part sea otters, the large California sheephead fish Semicossyphus indirectly (see Cowen etal., 1982; Foster, 1982). The pulcher (Cowen, 1983) and spiny lobster Panulirus inter- reversal occurred because direct effects of Storm I were ruptus (Tegner and Levin, 1983) may control urchin num- indirect effects of Storm II and vice versa: Storm I (1980) bers. Yet sheephead abundance at Naples Reef was destroyed kelp, which altered the feeding behavior of probably far less than that needed to control exposed urchins; Storm II (1983) decimated urchins, which allowed urchins (Cowen, 1983), and lobsters were overfished and successful recruitment of kelp. rare (own personal observations). After Storm I (February 1980), new kelp plants ap- Even though Storm II created as much or more dis- peared during spring and early summer when nutrient and turbance as Storm I, it had the reverse biological effect on light levels favor plant recruitment and growth (e.g. the reef community. Dense stands of kelp sporophytes Harger, 1979; Dean and Deysher, 1983). However, nearly appeared on new rock surfaces bared by the storm. Plant all were eaten by sea urchins, which had presumably settlement was unusually heavy, despite an uncertain emerged from rocky hiding places once located near ac- source of propagules and the presumed limited dispersal cumulations of drift kelp and smaller amounts of other distance of kelp spores (see Anderson and North, 1966; algae. Urchins are known to alter their feeding behavior Dayton, 1973). Wave action decimated the population of from quietly sheltering and holding drift, to moving about urchins because most individuals were foraging in the and grazing live plants when drift food is unavailable open and exposed to the full force of the surge. Without (Dean etal., 1984 and references therein; Harrold and grazing urchins, the young kelp plants survived and grew. Reed, 1984). At Naples the change was manifest as an Also, an initial cover of early-arriving, fast-growing fila- apparent doubling of urchin densities at our regularly mentous brown algae (Ectocarpus spp. and Giffordia spp.) monitored midreef site (Fig. 3: top graph), as we were also may have protected young kelp plants from grazing fish able to see and count the previously hidden individuals. (Harris etaL, t984). The kelp understory soon reached This high density of exposed sea urchins probably pre-disturbance (1979) levels of percent cover. exceeds that at which living plants can survive in the Although the density of kelp recruits was more than 10 absence of drift. Red urchins (Strongylocentrotus fran- times greater after Storm II than after Storm I, the lack of ciscanus) are larger and more active than purple urchins kelp regrowth after Storm I was more likely due to grazing (S. ])urpuratus). Leighton et al. (1966) concluded that algae urchins than to recruitment limitation. Wherever they can recolonize successfully among urchins whose densities survived Storm II, urchins were fully capable of destroying are not much more than 1 red urchin or 10 purple urchins even the densest stands of young kelp. For example, m -2, much less than we observed at midreef. Presumably, urchins that had survived under boulders within a surge A.W.Ebeling et al.: Storm disturbances of a kelp forest 293

shadow below Site NM soon moved upslope to eliminate sea urchins and aiding kelp recruitment. Thus, our findings sporophytes that had recruited heavily to extensive new suggest that if predators or other agencies control urchin surfaces there. numbers (see "Introduction"), storm effects should be Reefwide, kelps survived despite an E1 Nifio intrusion regenerative (Cowen etal., 1982; Foster, 1982). But in of warm, nutrient-poor water that has persisted since mature forests where urchin populations are poorly winter 1982-1983 off coastal southern California (Fiedler, regulated, severe storms may have degenerative effects 1984). As also observed off San Diego some 300 km to the because they eliminate the detritus base. south (Dayton and Tegner, 1984), however, water cooled to usual levels in spring 1983 indicating a strong pulse of Acknowledgements. We thank M. Foster, R. Larson, and D. upwelling and nutrient enrichment. This and intermittent Reed for reviewing the manuscript. A. DuBois, C. Ebeling, shoaling of the thermocline during the summer may have J. Jenkins, T, Miller, and T. Pearsons helped with field supplied plants with the nutrients required for canopy work. S. Anderson provided technical assistance with regrowth in spring 1984 (see Harger, 1979; North et al., equipment and boating operations. D. McLaren and R. 1982). Understory kelps and lower fronds of giant kelp Panza drafted illustrations. The Marine Science Institute may have been nourished from time to time by nutrient- supplied administrative services. The work was supported rich water below the thermocline. They grew new blades by NSF Grants OCE79-25008 and OCE82-08183. or fronds during the spring upwelling period, and formed well-developed surface and understory canopies by sum- Literature cited mer. Consequently baby surfperch, which require a cover of understory kelp for protection from piscivores, reap~ Anderson, E. K. and W. J. North: In situ studies of spore pro- duction and dispersal in the giant kelp Macrocystis. Proc. int. peared for the first time since deforestation after Storm I Seaweed Symp. 5, 73-86 (1966) (Ebeling and Laur, 1984). Drift kelp began to accumulate. Breen, P. A. and K. H. Mann: Destructive grazing of kelps by sea Hence, the remaining urchins were able to exploit a urchins in eastern Canada. J. Fish. Res. Bd Can. 33, 1278-1283 renewed detrital supply and reassume their sheltering (1976) mode. Connelt, J. H.: Diversity in tropical rain forests and coral reefs. Science, N.Y. 199, 1302-1310 (1978) Surfperch abundance apparently depended on outputs Connell, J. H. and W. P. Sousa: On the evidence needed to judge of the detritus-based food chain. The strong correlation of ecological stability or persistence. Am. Nat. 121, 789-824 adult numbers with algal-turf cover indicates that the fish (1983) were tracking their food supply of small prey that live in Cowen, R. K.: The effect of sheephead (Sernicossyphus pulcher) on red sea urchin (Strongylocentrotus franciscanus) turf (Laur and Ebeling, 1983; Stouder, 1983). Many of populations: an experimental analysis. Oecologia 58, 249-255 these prey, such as amphipods and crabs, are facultative (1983) detritivores, ingesting plant litter and other refuse coated Cowen, R. K., C. R. Agegian and M. S. Foster: The maintenance with bacterial slime (Mann, 1982). Before urchins had of community structure in a Central California giant kelp invaded our site, both turf cover and surfperch density forest. J. exp. mar. Biol. Ecol. 64, 189-201 (1982) Dayton, P. K.: Dispersion, dispersal, and persistence of the annual varied seasonally, increasing during the spring-summer intertidal alga, Postelsia palmaeformis Ruprecht. Ecology 54, productivity pulse (Fig. 3: bottom graph). Then both 433-438 (1973) remained at low levels during the extended barren period Dayton, P. K., V. Currie, T. Gerrodette, B. Keller, R. Rosenthal before Storm II. Overlap in microhabitat use between surf- and D. V. Tresca: Patch dynamics and stability of southern California kelp communities. Ecol. Monogr. (In press). (1984) perch species increased as fish congregated about the reef Dayton, P. K. and M. J. Tegner: Catastrophic storms, E1 Nifio, crest and adjacent slope where urchins were fewer and turf and patch stability in a southern California kelp community. persisted (Stouder, 1983). However, the predictable in- Science, N.Y. 224, 283-285 (1984) crease in turf and fish after Storm II was not fully realized, Dean, T. A. and L. E. Deysher: The effects of suspended solids because our site (Fig. 1, Site NM) was eventually overrun and thermal discharges on kelp. In: The effects of waste disposal on kelp communities, pp 114-135. Ed. by W. Bascom. by surviving urchins (see above). Long Beach, California: Southern California Coastal Water That severe storms may catalyze regenerative as well as Research Project 1983 degenerative processes may help explain what North Dean, T. A., S. C. Schroeter and J. D. Dixon: Effects of grazing by (1971) described as "irregular changes" in southern Cali- two species of sea urchins (Strongylocentrotusfranciscanus and Lytechinus anamensus) on recruitment and survival of two fornia kelp forests. In our example, Storm I set forth species of kelp (Macrocystis pyrifera and Pterygophora cali- processes disrupting the detritus-based food chain to the fornica). Mar. Biol. 78, 301-313 (1984) extent that the reef community was unable to resume its Duggins, D. O.: Kelp beds and sea otters: an experimental previous form. This happened despite the facts that (1) approach. Ecology 61, 447-453 (1980) winter-storm disturbances generally precede the season of Ebeling, A. W., R. J. Larson, W. S. Alevizon and R. N. Bray: Annual variability of reef-fish assemblages in kelp forests off maximum light and productivity (Harger, 1979; North Santa Barbara, California. Fish. Bull. U.S. 78, 361-377 (1980) et al., 1982), and (2) loss of the surface canopy of giant Ebeling, A. W. and D. R. Laur: The influence of plant cover on kelp allows light for understory growth that would other- surfperch abundance at an offshore temperate reef. Envir. wise be suppressed by shading (Foster, 1982; Dayton and Biol. Fish. (In press). (1984) Tegner, 1984; Dayton et al., 1984; Reed and Foster, 1984). Ebert, T. A.: Negative growth and longevity in the purple sea urchin Strongylocentrotus purpuratus (Stimpson). Science, Storm II reversed the degenerative process by removing N.Y. 157, 557-558 (1967) 294 A.W. Ebeling et al.: Storm disturbances of a kelp forest

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